Content uploaded by Armando Valdés-Velasquez
Author content
All content in this area was uploaded by Armando Valdés-Velasquez on Jun 30, 2016
Content may be subject to copyright.
15
Humboldt Penguin
(Spheniscus humboldti)
S D P, A B, M C,
A V-V, P M, A S
1. SpecieS (common and Scientific nameS)
Humboldt penguin, Spheniscus humboldti (Meyen,
).
e Humboldt penguin is also known as the Peru-
vian penguin and pingüino de Humboldt, pájaro bobo,
pájaro niño, pachanca, and patranca (Spanish).
2. deScription of the SpecieS
e Humboldt is a medium-size penguin, with body
length of – centimeters and body mass of approxi-
mately .–. kilograms, depending on breeding con-
dition, sex, and prey availability (Coker ; Murphy
; Zavalaga and Paredes a) (table .). Although
similar to the other Spheniscus penguins, Humboldts
have large fleshy margins at the base of the bill (UNEP
).
Sexes are similar in plumage, but males tend to be
larger than females (Zavalaga and Paredes a; Wal-
lace et al. ) (table .). e head is mostly black-
ish gray, with a white chin and a narrow white stripe
extending from the bill on each side of the crown,
looping over the eyes and broadening at the junction
with the white upper breast. e upperparts, flip-
pers, legs, feet, and tail tend to be blackish gray, while
most of the underparts are white (fig. ). Adults have
an inverted black horseshoe-shaped band extending
down the flank to the thigh, which is lacking on juve-
niles and chicks. Black feathers on the breast appear
as spots and are individually distinct. e Humboldt’s
bill is black with a gray transverse bar and a fleshy pink
area at the base that is especially prominent during the
breeding season. e irises of chicks and juveniles are
dark gray, becoming pale and then darkening with age,
turning reddish brown as they become adults (Scholten
). Juveniles are easily distinguished from adults by
the brownish plumage on their heads, grayer cheeks,
and lack of the white head stripe and black horseshoe-
shaped breast-band (fig. ).
fig. 1. Adult male Humboldt penguin at Punta San Juan, Peru. (P. D.
Boersma)
fig. 5. On Isla Chañaral, Chile, a Humboldt penguin stands in the desert
vegetation. (T. Mattern)
V. Banded penguinS: genuS SpheniScuS
Gender determination of free-ranging penguins
using discriminant functions of morphometric charac-
ters is accurate (–) but is hindered by geographic
variation and effects such as abnormal bill growth asso-
ciated with captivity (Zavalaga and Paredes a; Wal-
lace et al. ). e main characteristics used for sex
determination were bill length (BL), measured from
the point in the V where feathers start to the tip of the
culmen, which is hooked on the upper mandible; bill
depth (BD), measured dorso-ventrally at the nares or
nostrils; and the width of the head (WH), measured
from the crevice just posterior to the bulge behind the
eyes.
3. taxonomic StatuS
e genus Spheniscus has four closely related species
(Baker et al. ). An ancestral population of Sphe-
niscus on the Pacific coast may have split, forming the
Humboldt and the Galápagos penguins (Spheniscus
mendiculus). is dispersal event is consistent with
the flow of the Humboldt Current. Consensus on the
evolutionary history and dispersal of the Spheniscidae
across the globe has not been reached (Bertelli and
Giannini ; Baker et al. ; Ksepka et al. ).
e Humboldt penguin is monotypic (UNEP ),
although its wide latitudinal distribution (–º S)
should expose the species to different selective pres-
sures over its breeding range (Simeone et al. ).
Hybridization between Humboldt and Magellanic (S.
magellanicus) penguins in mixed colonies occurs in
southern Chile (Simeone et al. ).
Although there is evidence of strong colony and
nest fidelity from field observations (Teare et al. ),
penguins are also capable of dispersion (Culik and
Luna-Jorquera b; Wallace et al. ; Taylor et al.
). Satellite tracking of individuals in periods of
scarce prey availability showed that penguins moved
more than kilometers away from their home
colonies (Culik and Luna-Jorquera a). Genetic
evidence suggests that sharp episodic fluctuations in
climate, such as El Niño events, or human pressure can
change the relationship between breeding locations
and demography, making it impossible to view colonies
as separate entities (Schlosser et al. ). is con-
nectivity is perhaps the main reason that microsatellite
data show no evidence of bottlenecks or strong popula-
tion fragmentation, although the number of Humboldt
penguins has decreased dramatically over the past two
centuries (Schlosser et al. ).
4. range and diStriBution
At least colonies have been described between Foca
(°΄ S) and Metalqui (°΄ S) ( in Peru and in
Chile) (table ., fig. ). Most of the breeding popu-
lation is located in Chile, but recent estimates suggest
an increase in the overall population (McGill et al.,
unpubl. data). Great uncertainty resulting from inaccu-
rate counting methods and fragmented and uncoordi-
nated counts throughout the Humboldt’s distribution
make a population estimate problematic.
In Peru, most of the population was concentrated
in five sites in – (Paredes et al. ) (table
fig. 2. Adult Humboldt penguins
and a juvenile Humboldt penguin
(lower right) rest on a guano island
in Peru. (P. D. Boersma)
humBoldt penguin (SpheniScuS humboldti)
.a), and in – (Majluf, unpubl. data). e –
El Niño, with high surface water temperatures that
altered prey distribution, and increased human pres-
ence and activities in the central coastal areas of Peru
may have caused the penguins’ clustered distribution
(Paredes et al. ). In Chile, the most important
breeding colony, with about , penguins, is at Isla
Chañaral (table .b) (Mattern et al. ).
Since the early s, colonies between –° south
are stable, with , birds. At the best-studied pen-
guin-breeding colony in Peru, Punta San Juan (°΄
S), El Niño events were followed by drastic reductions
in Humboldt populations (Majluf et al. ); penguins
slowly recovered (table .). At present, Punta San Juan
is the largest colony in Peru, with a total of , adult
birds (fig. ) (Cardeña and Bussalleu, unpubl. data).
In Chile (–° S), declines following El Niño
events were not as great as in Peru, and populations
likewise recovered. e increased number of penguins
in the time series in Chile is likely due not to more
penguins but to a change in census methodology that
allowed greater accuracy in describing the Humboldt
population at Isla Chañaral (°΄ S) (Mattern et al.
). e southernmost colonies (–° S) are small
and, since the s, stable.
Although restricted to Peru and Chile, Humboldt
penguins have been found in the wild in the Northern
Hemisphere on several occasions. One was caught by a
herring fisher in Alaska and released, but it likely had
been transported by boat (Van Buren and Boersma
).
5. Summary of population trendS
Humboldts have declined since the th century (Mur-
phy ), with a marked reduction after the –
El Niño event, leaving no more than , penguins
(Duffy et al. ; Hays ; Araya and Todd ). A
decade later, the population was estimated at ,–
, (Boersma et al. ).
Increases in numbers continued in the s but
were regarded skeptically by some researchers. Paredes
et al. () suggest that increases in Peruvian counts
were masking a process of population clustering, leav-
ing the species vulnerable to catastrophes ( of the
Peruvian population was found in San Juan, San Juan-
ito, Hornillos, Pachacamac, and Tres Puertas).
In Chile, numbers also increased (Simeone et al.
). However, the confirmation of , penguins
in Isla Chañaral in was a surprise (Mattern et al.
), as it was more than the total estimated popula-
tion. is number was the product of inconsistent cen-
sus methods rather than a real population increase.
Later estimates range between , to ,
breeding birds (Boersma ). Other recent esti-
mates describe a total population of , individuals
(Schlosser et al. ); however, this number is based
on an expert’s opinion and not on field data, highlight-
ing the absence, obsolescence, and fragmented nature
of accurate census data and the difficulty of counting
this species along the coast.
e Isla Chañaral counts stress that estimated pop-
ulation size is closely related to the census methodol-
fig. 3. Distribution and abundance of
the Humboldt penguin.
V. Banded penguinS: genuS SpheniScuS
ogy used (Mattern et al. ). An efficient method for
counting these birds is a pressing need (fig. ) (Araya et
al. ; Luna-Jorquera et al. ; UNEP ; Mat-
tern et al. ; BirdLife International ).
Recent improvements in census methodologies
have led to more accurate counts (Mattern et al. )
but may not indicate increases in the global population
(BirdLife International, ). After all, the magnitude
of possible positive population trends in recent years
will be masked by decades of underestimations (Mat-
tern et al. ).
In Punta San Juan since the early s, the penguins
have been counted twice during the breeding season
and once during the molt. e largest count is during
the molt and at the peak of breeding in May (Cardeña
et al., unpubl. data). For large-scale counts across the
Humboldt’s entire distribution, Luna-Jorquera et al.
() suggests counting penguins on the beach just
above where the waves are breaking between :
and : .
Ideally, as Boersma () suggests, each penguin
colony should be visited at least annually.
6. iucn StatuS
e International Union for Conservation of Nature
lists the Humboldt penguin as Vulnerable on its Red
List of reatened Species because the species has
undergone extreme population size fluctuations and
decline (IUCN ). Local estimates and expert opin-
ions suggest that the Humboldt is slowly bouncing
back. e status of Vulnerable is justified, as the popu-
lation has not reached historical numbers of “hundreds
of thousands” (Murphy ), it is clustered (Paredes
et al. ; Simeone et al. ), and major threats to
the species (e.g., overfishing, entanglement in gill nets,
habitat destruction) have not been ameliorated.
Nevertheless, actions have been taken toward
increasing the protection of Humboldt breeding colo-
nies in Peru through the Decreto Supremo –-
MINAM and in Chile (Simeone et al. ; UNEP
) and reducing the impact of guano-harvesting
methods at the penguins’ largest colony in Peru at
Punta San Juan (Majluf, unpubl. data). Both countries
have implemented the Convention on International
fig. 4. Humboldt penguins at Punta San Juan, Peru, rest on the coast. (P. D. Boersma)
humBoldt penguin (SpheniScuS humboldti)
Trade in Endangered Species of Wild Flora and Fauna
(CITES) under national law (Paredes et al. ; Iriarte
).
e Humboldt penguin is legally protected through-
out its distribution (table .). Peruvian legislation,
Decreto Supremo –-AG, prohibits the hunting,
possession, capture, transportation, and export of the
birds for commercial purposes and categorizes the
species as Endangered in Decreto Supremo –-
AG. Chile implemented a -year hunting ban, Decreto
Supremo , in , and since , Decreto Supremo
forbids hunting, transport, possession, and com-
mercialization of penguins (Iriarte ). Chile adopted
a new species-categorization system for conserva-
tion, granting legal status to international categories
but interpreting them locally; thus, Decreto Supremo
/ ranks the Humboldt penguin as “vulnerable.”
Most of the penguins breed within protected areas
in Peru and Chile: Pingüino de Humboldt National
Reserve, Isla Cachagua Natural Monument, Islotes de
Puñihuil National Monument, Guano System National
Reserve (officially established in January ), the
Paracas National Reserve, and the San Fernando
National Reserve (UNEP ; SPIJ ).
7. natural hiStory
Breeding Biology. e breeding period starts right after
the molt (Zavalaga and Paredes b). Nest selection
and occupation begins when penguins return to their
breeding colonies after an extended period of foraging
and recovery at sea (Zavalaga and Paredes b; Sime-
one et al. ).
Humboldt penguins nest on cliff tops, beaches, and
scrapes covered by vegetation and in sea caves, rock
crevices (fig. ), and burrows dug into dirt or guano
(Simeone and Schlatter ; Battistini and Paredes
; Simeone and Bernal ; Paredes and Zavalaga
).
Surface nests are common in areas without terres-
trial predators and with little human disturbance (fig.
) (Paredes and Zavalaga ). In Punta San Juan,
penguins in surface nests endure persistent cool winds,
sea breezes, and shade through the year, as these coun-
teract the high solar radiation on hot days. Penguins at
Pájaro Niño nest in dirt burrows and rock crevices that
offer protection from solar radiation and egg predators
(Simeone and Bernal ).
Humboldts breed throughout the year when
resources are abundant (Battistini ; Paredes and
Zavalaga ; Paredes et al. ; Simeone et al.
). In Punta San Juan, reproduction occurs from
March to December (Paredes and Zavalaga ),
with two prominent reproductive peaks in April–May
and August–September (Paredes and Zavalaga ;
Cardeña et al., unpubl. data). In central Chile, there
are also two reproductive peaks, but offset by a month
(May, October), and the number of nests depends on
fig. 6. Adult Humboldt penguin
on a rock crevice with two eggs
at Algarrobo Island, Chile. (P. D.
Boersma).
fig. 7. Humboldt penguins breed-
ing on Isla Chañaral, Chile. (T.
Mattern)
V. Banded penguinS: genuS SpheniScuS
prey availability and climatic factors such as rainfall
(Simeone et al. ).
Females lay two eggs days apart and of similar size
(see table .). Incubation lasts for six weeks (approx.
– days). Hatching, like egg laying, is – days
apart (Deeming et al. ; Paredes et al. ).
Based on recovery of banded birds at Pajaro Niño
in central Chile, age at first breeding ranges from . to
. years (mean = ± year, n = [A. Simeone, unpubl.
data]). Araya et al. () suggest that first reproduc-
tion takes place or years after hatching, as fledg-
lings are not sexually mature. Humboldt penguins on
Pajaro Niño tend to breed in nests within – meters
of their natal nests, and most use the same nest type
as their natal nests when they first breed (A. Simeone,
unpubl. data).
Chick rearing takes – weeks (approx. days)
until fledging (Paredes et al. ). e whole process
from incubation to fledging lasts for approximately
days (Paredes and Zavalaga ). Both parents take
turns foraging at sea and feeding the chicks (fig. )
(Luna-Jorquera and Culik ; Taylor et al. ; Hen-
nicke and Culik ).
In southern Peru, double brooding is common
(approx. [Paredes et al. ]) (fig. ). In north-
ern-central Chile (–° S), parents rarely raise both
chicks (Simeone et al. ). Breeding success (fledg-
lings per nest) varies within and among years and sites.
At Punta San Juan, however, breeding success averaged
around one chick: . ± . in (n = ) and .
± . in (n = ) (Paredes and Zavalaga ).
Although this species is monogamous, extra-pair
mating and copulation occurred but failed to result in
young (Schwartz et al. ).
foraging BehaVior and prey. Humboldts are pelagic
predators (Luna-Jorquera and Culik ) and prob-
ably visual hunters (Martin and Young ). ey
may use smell to recognize areas of high productivity
and conspecifics (Coffin et al. ). Nonetheless, their
foraging rhythm depends on light intensity, and dive
depths in excess of meters are uncommon (Taylor
et al. ).
Humboldts feed close to their breeding colonies
during reproduction, within a radius of about kilo-
meters (Culik et al. ; Luna-Jorquera and Culik ;
Boersma et al ). As for other penguins, their for-
aging distance is estimated by how long they are gone
(Boersma et al. ). ey follow pelagic shoals or
are found foraging in loose aggregations, even engag-
ing in solitary foraging, which is rare among Peruvian
seabirds (Duffy ). eir main target species vary
depending on location and prey availability (Wilson
et al. ; Herling et al. ). Frequent prey include
anchovies, silversides, and jack mackerel, among oth-
ers (table .). Cephalopods such as Patagonian squid
(Loligo gahi), Southern Ocean squid (Todarodes filip-
povae), and Humboldt squid (Dosidiscus gigas), and
crustaceans (isopods and stomatopods) have also been
described as parts of their diet (Wilson et al. ; Her-
ling et al. ).
e Humboldt’s foraging effort is directly propor-
tional to foraging distance traveled and average dive
depth. Energy investment during foraging varies with
fig. 8. Humboldt penguin chick waits at its nest for its parents to return and
is nearly ready to fledge. (T. Mattern)
fig. 9. Adult Humboldt penguin in a nest site with two chicks marked with
fiber bands at Punta San Juan, Peru. (P. D. Boersma)
humBoldt penguin (SpheniScuS humboldti)
food scarcity. During El Niño events, energy investment
doubles to kilojoules spent per day, compared to
kilojoules spent per day before the El Niño event
(Culik et al. ). Penguins must eat at least –
grams of anchovies per day just to cope with the energy
costs of foraging (Luna-Jorquera and Culik ). As
cephalopods have a lower energy content than fish, the
greater the proportion of cephalopods in the penguins’
diet, the lower the energy per stomach load (Herling et
al. ).
predatorS. Little is known about predators of the Hum-
boldt. Williams () states that killer whales (Orcinus
orca), great white sharks (Charcarodon charcarias),
and South American fur seals (Arctocephalus australis)
prey on Humboldt penguins at sea. e South Ameri-
can sea lion (Otaria flavescens) kills penguins at sea
and on the shore (Cardeña, pers. obs.). Desert foxes
(Lycalopex sechurae) are the main predators of adults,
juveniles, and chicks on land (Williams ). Without
the walls that exclude foxes from Punta San Juan, few
penguins would survive; for example, a single desert
fox entered in and killed approximately adult
penguins in just two days (Cadeña, pers. obs.). Peruvian
gulls (Larus belcheri) and kelp gulls (Larus dominica-
nus) prey on the eggs (Wilson et al. ; Paredes and
Zavalaga ). Vampire bats (Desmodus rotundus) are
also micro-predators of this species, biting the feet and
tarsometatarsi of chicks and juveniles (Luna-Jorquera
and Culik ). Introduced predators such as dogs
(Canis familiaris) kill adults; rats (Rattus rattus) prey
on eggs, but their impact is not uniform and depends
on location and year (Simeone and Bernal ).
molt. e penguins’ feathers protect their skin against
water and work as an insulator. During molt, Hum-
boldt penguins do not enter the sea to forage (Pare-
des et al. ; Otsuka et al. ). To allow for an
energy-demanding molt and a period of forced fast-
ing, they become hyperphagic during the pre-molting
period and then return to the colonies to replace their
entire plumage over a short period of time (Zavalaga
and Paredes b; Paredes et al. ). is process
is closely related to circulating thyroxine, testosterone,
and estradiol levels; increases of thyroxine in conjunc-
tion with low levels of testosterone and estradiol might
trigger feather growth (Otsuka et al. ).
Molting initiation and duration vary with latitude
(Scholten ; Zavalaga and Paredes b; Luna-
Jorquera et al. ; Paredes et al. ; Simeone et
al. ). Adult molting in southern Peru (–º S)
lasts for approximately days, peaking between Janu-
ary and February (Paredes et al. ), while in north-
central Chile, the peak of molting tends to be one
month later (Simeone et al. ). Captive penguins in
the Northern Hemisphere start molting in July, reflect-
ing that hemisphere’s solar radiation and photoperiod
(Schloten ), and have shown shorter molting peri-
ods ( days), perhaps because of more constant food.
annual cycle. Humboldts have two breeding peaks, but
breeding depends on prey availability and can cease,
with penguins deserting their nests during strong El
Niño periods (fig. ).
8. population SizeS and trendS
Although the Humboldt population has severely
declined since the th century and showed marked
reductions after the – and – El Niños, the
population is now increasing slowly. Some authors esti-
mate a population of , breeding adults (Schlosser
et al. ); however, these are based not on actual
counts but on the opinions of researchers.
As population numbers are prone to fluctuate in
relation to changes in prey availability (El Niño events)
and interactions with fisheries, recent improvements in
Peruvian counts could be a result of a fixed escapement
March
April
May
JuneJuly
August
September
October
November
December
February
January
fig. 10. Annual cycle of the Humboldt penguin.
V. Banded penguinS: genuS SpheniScuS
policy of million tons of spawning biomass (Guevarra-
Carrasco et al. ) for Peruvian anchoveta (Engraulis
ringens) and the recent implementation of an individual
transferable quota system for fisheries established by
Decreto Legislativo . Nevertheless, it is a priority
to assess the impact of these policies on the conserva-
tion of penguins and other anchovy-dependent fauna.
In terms of actual population numbers, field data on
species abundance are scarce and of limited accuracy.
Counting methodologies are inconsistent (perhaps
masking the Chilean trends), and species monitoring
is concentrated in just a few sites, neglecting newly dis-
covered colonies (Bussalleu, pers. obs.).
9. main threatS
reats to Humboldt populations are shown in table
.. Most of the threats described in the s are still
major concerns today (Murphy ; Boersma and
Stokes ; BirdLife International ).
el niño and climate Variation. e Humboldt Current
upwelling system has alternating blooms and deple-
tions of productivity triggered by Kelvin waves com-
ing into contact with the South American Pacific coast
(Bertrand et al. b). El Niño events, recurring peri-
ods of reduced upwelling intensity, increase the average
depth of pelagic schools of Peruvian anchoveta (Ber-
trand et al. a) and thus reduce prey availability
(Culik et al. ; Taylor et al. ) and increase adult
penguin mortality.
Together with other environmental changes asso-
ciated with Kelvin waves (such as increased rainfall
leading to the collapse of nests), increases in nest aban-
donment and chick mortality during El Niño events
have alarmed researchers in Ecuador, Peru, and Chile
(Boersma ; Paredes and Zavalaga ; Simeone et
al. ).
Species inhabiting the Humboldt Current have sur-
vived periods of food scarcity, but the increased fre-
quency of El Niño events likely will harm the Humboldt
penguin as it has the Galápagos penguin (Boersma
; Vargas et al. ). Dramatic increases in fish-
ing effort (ongoing since the s) modify energetic
and nutritional flows across the trophic webs, reducing
the carbon flux toward top predators, such as seabirds
(Jahncke et al. ). e introduction of large-scale
industrial fisheries increases the ecosystems’ vulner-
ability and can lead to losses in biodiversity and even
ecological collapse (Pauly et al. ; Cury et al. ;
Pauly and Palomares ). As the commercial fisher-
ies of Chile and Peru intensively exploit the Humboldt’s
main prey species, it is thought that this competition is
the most pressing threat to the species’ conservation,
hindering its ability to recover population sizes similar
to those of the th century (Duffy et al. ; Herling
et al. ; BirdLife International ).
fiShing. Bycatch in the small-scale fisheries in Peru and
Chile is an ongoing problem (Duffy ; Simeone et
al. ; Majluf et al. ; Melly et al. ; Boersma
et al. ). Most of the penguins’ foraging activities
take place within a radius of kilometers around their
colonies and in depths of less than meters (Culik et
al. ; Luna-Jorquera and Culik ; Taylor et al.
; Boersma et al. ); thus, they are vulnerable to
entanglement in fishing nets that target pelagic com-
mercial species (Boersma and Stokes ; Simeone et
al. ; Majluf et al. ; Taylor et al. ; Melly et
al. ). For example, at least , penguins (about
of the overall estimated population size at the
time) were bycatch in gill nets of small-scale fisheries
between and in Chile and Peru (Simeone et
al. ; Majluf et al. ). eir accidental drownings
were associated mostly with drift gill nets in fisheries
targeting palm ruffs (Seriolella violacea) and corvina
drums (Cilus gilberti).
Mesh size and fishing methods may change rates of
penguin mortality. It seems that penguins are entangled
while resting at sea at night after foraging or while they
are approaching anchovy schools during the day (Duffy
; Simeone et al. ; Majluf et al. ; Taylor et
al. ; Boersma et al. ). Some authors have sug-
gested banning drift gill nets at night and establishing
no-take zones in areas within kilometers of breeding
colonies (Taylor et al. ; Boersma et al. ), but
there has been little response from Chilean and Peru-
vian authorities. Other authors are deeply concerned
with this issue, as local depletion of valuable fish con-
tinues to force artisanal fishermen to change target fish
and shellfish species and seek new fishing grounds,
often around penguin rookeries (Paredes et al. ).
guano harVeSting. Guano harvesting is detrimental to
the conservation of penguins (Boersma and Stokes
humBoldt penguin (SpheniScuS humboldti)
). It is important to note that there are nevertheless
examples of sustainable, less harmful harvests in Punta
San Juan (Majluf et al., unpubl. data). Peruvian guano is
a valued organic fertilizer derived from the excrement
of the Guanay cormorant (Phalacrocorax bougainvil-
lii), Peruvian booby (Sula variegata), and Peruvian pel-
ican (Pelecanus thagus), and the fecal deposits of these
birds are the nesting substrates for Humboldt penguins
in Peru (fig. ) (Boersma and Stokes ; Battistini
; Battistini and Paredes ; Paredes and Zavalaga
).
us, guano harvesting reduces nesting habitat for
penguins (Murphy ; Duffy et al. ; Boersma and
Stokes ; Paredes et al. ), but guano miners also
increase adult and egg mortality through direct harvest
and by the introduction of alien species such as dogs
and rats (Duffy et al. ). Even without guano har-
vest, human presence has harmed colonies (Simeone
and Bernal ) through the introduction of species
such as goats that trample nests (Simeone and Schlat-
ter ).
haBitat loSS. Coastal development reduces breed-
ing sites (Duffy et al. ; Araya et al. ). e
increased human presence near Humboldt colonies
is of concern because these penguins are among the
timid species of the Sphenisciformes (Ellenberg et al.
). Habituation is possible, but visual contact with
humans increases their heart rate and can result in
nest abandonment (Taylor et al. ; Ellenberg et al.
). Unregulated tourism is problematic for the spe-
cies (Simeone and Schlatte ; Ellenberg et al. ;
Skewgar et al. ); however, its impacts on breeding
success, attendance, and mortality are not quantified.
diSeaSe. Changes in coastal use (e.g., increased chicken
aviculture) are a possible driver for new diseases that
could further endanger the species (Duffy et al. ;
Adkesson, pers. comm.), but impacts on penguin
health are not quantified (Smith et al. ). A team
of veterinary researchers led by Michael Adkesson is
quantifying changes in pathogens, diseases, viruses,
and pollutants that were previously described at Punta
San Juan in Smith et al. ().
10. recommended priority reSearch
actionS for conSerVation
Research can aid in conserving this species. e follow-
ing actions address the most pressing needs:
. Define a consolidated census methodology. What
are the optimum survey times and methods for
determining the population size of the species
across its distribution?
. Monitor distribution and abundance. How many
penguins are there? How do colonies behave in
periods of food abundance and scarcity?
. Quantify the impact of human activities (urban
fig. 11. At Punta San Juan, Peru,
Humboldt penguins dig burrows in
the guano to nest. (P. D. Boersma)
V. Banded penguinS: genuS SpheniScuS
growth, tourism, industrial fishing, small-scale fish-
ing, mining, farming, animal husbandry) on distri-
bution, abundance, and breeding success.
. Identify and quantify the impacts of climate change
on population size, distribution, and breeding suc-
cess.
. Identify critical areas for conservation. Which colo-
nies are facing the worst pressures? Where are pen-
guins most prolific? What areas do penguins use for
transit and migration? Where should marine pro-
tected areas (MPAs) or zoning for conservation be
located?
. Generate relevant information for industrial fish-
ery management and policy (define catch quotas
and fishery bans based on ecosystem parameters).
Monitor targeted prey species and their relative
contribution (numbers, mass, and energy) to the
penguins’ diet.
. Generate a baseline of health parameters across
the Humboldt penguin’s distribution. What are
the most common pathogens, parasites, and dis-
eases? How do they affect the penguins’ mortality
and reproductive success? Are there areas where or
times when penguins are more prone to diseases?
. Assess the impacts of MPAs on penguin conser-
vation. Does the current MPA system protect the
species? Have population sizes and breeding suc-
cess improved after the establishment of protected
areas? Do reductions in harvests of fish result in
increases in numbers of penguins and other sea-
birds?
. Develop innovative educational programs on for-
age fish and seabird conservation for adult and
childhood education on forage fish and seabird
conservation to better understand economic and
conservation trades-offs with human well-being.
Conservation programs should include interactive
websites, talks in schools, TV presentations, and
community-based projects.
11. current conSerVation effortS
Humboldt penguins are protected by MPAs (marine
reserves, marine parks, natural monuments, national
reserves, and reserved zones). Some protect marine
extensions (foraging habitats), others land (nesting
habitats), and some both. eir effectiveness is related
to the ability of the Peruvian and Chilean governments
to properly enforce conservation measures against
urgent threats and short-term economic gain. is
capacity is limited and perhaps insufficient. Moreover,
although some breeding sites are protected, many areas
lack appropriate participatory management plans that
include Humboldts as an object of conservation (Skew-
gar et al. ) (fig. ).
In January , the Peruvian government estab-
lished the Guano System National Reserve (Decreto
Supremo –-MINAM) (Ministerio del Ambi-
ente ). is network of headlands, capes, and
islands harbors Humboldt nesting sites and protects
major foraging areas around them. e San Fernando
National Reserve (established in July by the
Decreto Supremo –-MINAM) is also a major
site for penguins.
It is also important to highlight that Isla Chañaral,
the main breeding colony for the species, is protected
(UNEP ) and that improvements in MPA cover-
age and management are significant in Chile (Pizarro
).
fig. 12. Adult Humboldt penguin at its nest on Isla Choros, Chile. (T.
Mattern)
humBoldt penguin (SpheniScuS humboldti)
Establishing sustainable guano harvest method-
ologies, implementing protective tourism routes with
camouflaged observation points, removing alien spe-
cies from breeding sites, enforcing fishery no-take
zones around breeding colonies, and applying the eco-
system approach to fisheries (Garcia et al. ) are all
major challenges for the future of the species.
12. recommended priority conSerVation actionS
In general, information on species distribution and
abundance is needed. Census methodologies for Chile
and Peru should be unified and a complete penguin
count made over the range of the species (Araya et al.
). Additional recommendations include the fol-
lowing specific actions:
. Acquire information on abundance, breeding phe-
nology, reproductive success, and adult mortality
for the most representative reproductive colonies
at least once a year and perhaps conduct a full cen-
sus across the species’ range once every three to
four years (Boersma ).
. Determine migratory and transit corridors between
colonies by means of ecological and genetic studies
(Schlosser et al. ).
. Implement a sustainable guano harvest method,
to minimize disturbance at the breeding colonies
and better preserve nesting habitat, as was done
for two guano harvests at Punta San Juan (Majluf,
unpubl. data). e guano sites in Peru are part of a
national reserve, and tools developed at Punta San
Juan should be incorporated into guano manage-
ment plans for all sites. Promote compliance with
protective guano harvesting guidelines as a part of
national and regional regulations.
. e industrial anchovy fishery is a threat to Hum-
boldt penguins and other seabirds, so total allow-
able catches should be set based on trophic and
oceanographic models that include ecological
parameters (such as prey dependence) (Chris-
tensen and Walters ; Cury et al. ). Include
a precautionary approach to uncertainty in fishery
policy (Ward et al. ), reducing fishing pressure
during El Niño events.
. Monitoring of bycatch and fishing efforts is critical
for penguin conservation (Majluf et al. ; Melly
et al. ; Skewgar et al. ). Monitor fishing
areas and landings of small-scale and artisanal fish-
eries for areas and gear that render the greatest
bycatch. Vessel monitoring and landing data would
also provide a description of spatial and resource
use patterns for these small-scale fisheries around
breeding colonies.
. Use these data to inform zoning proposals (fishing
areas, no-take zone, areas where only hook and line
are allowed, etc.) and fishing policies (fishing bans,
mesh sizes, catch shares, etc.) that could enhance
conservation of commercially targeted species and
reduce disturbance to Humboldt breeding colo-
nies (Araya et al. ). Local stakeholders need
to be involved in these activities, which should be
coupled with educational and outreach programs
that will enhance their ability (Olsen et al. ) to
reduce bycatch, improve self-governance, and con-
vince local stakeholders to accept MPAs and com-
ply with their regulations.
. Implement on-board observer programs for obtain-
ing data on bycatch. Integrating this information
with satellite data from vessel monitoring programs
and GPS tracking and telemetry data from projects
studying the Humboldt’s foraging areas will provide
a better sense of how, if, and when industrial fisher-
ies cause local depletions of prey. is information
could then be used for rapid adaptive management
so that fishing policies and activities can minimize
their impact in key areas during the species’ breed-
ing seasons.
. Many MPAs have been established across this spe-
cies’ distribution and include important breeding
colonies. Enforcement of these protections should
be coupled with management plans that have
clearly defined, measurable objectives so that con-
servation practitioners can monitor the efficiency
of MPAs in relation to Humboldt penguins (Skew-
gar et al. ) and adapt to changes as necessary
(e.g., assess the effectiveness of a no-take zone after
a predetermined period of time).
. Include capacity building and local involvement
of stakeholders from civil society when discussing
sustainable practices and policies intended to help
conserve marine biodiversity (Olsen et al. ),
including especially the Humboldt penguin. Initi-
ate efforts to communicate science in more novel
ways that can better reach target stakeholders like
V. Banded penguinS: genuS SpheniScuS
fishermen and policy makers.
Other conservation activities include developing
clearly defined regulations on tourism in MPAs and
near penguin breeding sites and including these regu-
lations in regional conservation action plans, to reduce
negative impacts on the species; enhancing waste
treatment efforts in coastal regions where mining,
industries, and urban areas are located near breeding
colonies; and implementing health-monitoring pro-
grams at breeding colonies.
acknowledgmentS
We thank the Chicago Zoological Society, the Saint
Louis Zoo, and the Philadelphia Zoo for funding our
research and conservation efforts at Punta San Juan
during the past decade. e Chicago Zoological Soci-
ety and the Saint Louis Zoo are also currently sponsor-
ing Humboldt penguin health-monitoring programs
for wild populations, Humboldt colony identification,
and population size surveys across the species distribu-
tion. Moreover, we would like to thank P. D. Boersma
and P. Garcia Borboroglu for entrusting this task to our
team and for their patience.
taBle 15.1 Mean measurements of adult Humboldts
Site gender Bm wh Bl Bd fl data Source
Wild penguins at
Punta San Juan
Colo ny 1992 –1994
Males (n=165) 4711.06 ± 31.55 (g) Zavalaga and
Par edes (1997a)
Females (n=123) 4047.39 ± 35.15 (g)
Pooled (n=288) 4427.62 ± 30.42
(g)
Captive penguins
at Washington
Park Zoo
Male s (n=19) 4802.6 ± 10 0.5 (g) 5.49 ± 0.045 (cm) 6 .44 ± 0.075 (cm) 2.97 ± 0.04 5 (cm) Zavalaga and
Par edes (1997a)
Females (n=16) 4328.0 ± 92.6 (g) 5.22 ± 0.055 (cm) 6.03 ± 0.057 (cm) 2.71 ± 0.004 (cm)
Pool ed (n=35) 4585.7± 79.2 (g) 5.36 ± 0.0 42 (cm) 6.25 ± 0.059 (cm) 2.85 ± 0.037 (cm)
Dead penguins
recovered at
San Pedro Port
1992–19 93
Ma les ( n=112) * 4931.08 ± 56.05
(g) 5.13 ± 0.02 (cm) 6.5 4 ± 0.02 (cm) 2. 56 ± 0.01 (cm) 15.63 ± 0.06 (cm) Zavalaga and
Par edes (1997a)
Fe ma les ( n=111)* 4317.85 ± 52.15 (g) 4.75 ± 0.02 (cm) 6.08 ± 0.02 (cm) 2.27 ± 0.01 (cm) 14.93 ± 0.05 (cm)
Pool ed (n=223) 4643.54 ± 4 3.90 (g) 4.92 ± 0.02 (cm) 6.31 ± 0.02 (cm) 2.42 ± 0.01 (cm)
Wild penguins at
Pájaro Niño Colony
1994 –1995
Males (n=388) 65.21 ± 2.61 (mm) 27.59 ± 1.38 (mm) 216.67 ± 6.92
(mm)
Wallace et al.
(2008)
Females (n=368) 61.42 ± 2.45 (mm) 24.68 ± 1.48 (mm) 209.07 ± 7.63
(mm)
Note: e measurements taken where Body mass (BM), Length of head (LH), Width of head (WH), Bill length (BL), Bill depth (DB) and Flipper length
(FL). Data from Zavalaga and Paredes ( a) is presented as mean value in centimetres ± the standard error, whilst data from Wallace et al. ()
is presented as mean value in millimetres ± the standard deviation. Strong differences in FL measurements are due to methodological differences. For
Wallace et al. () FL was measured from the tip of the flipper to its junction with the thoracic wall, when the flipper was held perpendicular to the
sagittal plane of the body. For Zavalaga and Paredes ( a) FL was measured from the humero-radial joint to the tip of the flipper (maximum flattened
chord). *Only penguins ( males and females) were measured for the FL parameter.
taBle 15.2 Gender determination of Humboldts
zaValaga and paredeS (1997 a) wallace et al. (2008)
D = 3.16(WH) + 3.69 (BL)–38.98 Ln (P/(1- P)) = 42.889 –0.244(BL) –1–052( BD)
If D >0 the penguin was classied as mal e. P = e(42.889–0.244 BL–1–052 BD)
1+ e (42.889–0.244 BL–1–052 BD)
P is the probability that the penguin is female
(if P ≥ 0.5, the penguin is femal e).
Note: Bill length (BL), bill depth (BD), and width of the head (WH)
humBoldt penguin (SpheniScuS humboldti)
taBle 15.3 (a) Humboldt colonies in Peru
SiteS lat. ºS 1980 1981 1996 1997 1999 2000 2001 2002 2003 2004 2005 2006 2007 2008 2009 referenceS
Foca 05 º12 20 20 25 0 8, 12
Aguja 05 º41' 10 20 20 1, 12
Lobos de Tierra 06º25' 1000 900 100 00 35 0 1, 4, 8
Macabi 07º48 ' 15 1
Guañape Norte 0 8º32' 20 20 43 0 8, 12
Huarmey 10º04' 00 300 0 8
Mazorca 11º2 2 ' 150 120 10 0 1, 4
Pachacamac 12º 18' 600 75 0 800 230 575 959 120 1, 4, 8, 12
Santa María 12º18' 03 12
Asia 12º47 ' 00 227 206 8
Chincha Norte 13º3 8' 50 0 146 145 168 1, 8, 12
Ballestas 13º4 4' 9 60 79 153 157 98 1, 4, 8, 12
Culebras 13º 50' 46 0 12
San Gallán 13º 51' 111 60 191 259 192 101 1, 4, 8, 12
Tambillo 13º51 ' 33 12
Arquillo 13º 52' 50 1
Mendieta- Paracas 14º 03' 15 0 00 8, 12
Independencia 14º10' 010 12
Tres Puertas 14º10' 220 900 145 110 8, 12
La vieja 14º17' 8 00 1, 4, 12
Santa Rosa 14º19' 0 01 309 131 1, 8, 12
Gallinazo 15º0 9' 04 12
San Fernando 15º 09 ' 500 3 25 22 67 1, 8, 12
San Juanito 15º16' 505 538 812 917 8, 12
San Juan 15º22' 3680 2220 3650 3686 1631 1774 801 13 88 2305 14 07 2267 3214 25 45 3199 4421 1, 4, 8, 10–12, 19
Sombrerillo 15º3 0' 113 0 49 80 8, 12
Pampa Redonda 15º50' 1800 300 1, 4
La Chira 16º29' 300 60 1, 12
Caleta 16º 31' 93 133 12 0 79 8, 12
La Norte 16º31' 40 12
Quilca 16º43 ' 15 0 12
Honoratos 16º52 ' 417 12
Hornillos 16º5 3' 60 512 502 298 492 1, 8, 12
Carrizales 16º5 5' 23 0 16 14 8, 12
Tar pu y 16º58' 60 12
Islay 17º 01' 00 13 37 8
Cocotea 17º 15' 10 3 160 12
Cordel 17º1 5' 21 160 68 163 8
Corio 17º 15' 90 12
Platanales 17º 24' 026 12
Coles 17º4 2' 178 91 289 146 8, 12
e Maximum Recorded Values (individuals) for each year were extracted for all of Table II (a and b) from: () Araya et al.,; () Culik and Luna-
Jorquera, b; () Cursach et al., ; () Duffy et al., ; () Hertel et al., ; () Hiriart-Bertrand et al,. , () Luna-Jorquera and Cortes, ;
() Majlufunpublished data; () Mattern et al., ; () Paredes and Zavalaga, ; () Paredes et al., ; () Paredes et al., ; () Simeone,
; () Simeone and Schlatter, ; () Simeone et al., ; () Simeone et al., ; () Simeone et al., ; () iel et al., ; () UNEP,
.
V. Banded penguinS: genuS SpheniScuS
taBle15.3 (B) Humboldt colonies in Chile
SiteS lat. ºS 1981 1982 1983 1984 1985 1986 1987 1988 1989 1990 1991 1995 1996 1997 2000 2002 2003 2005 2008 2009 ref.’S
Cueva del
Caballo
20º 12' 16 1
Pan de
Azúcar
26º09' 6000 131 2500 2570 4000 600 1000 5900 1750 1, 2
Grande 27º15' 58 34 40 300 4270 4570 1, 7,
16, 18
Cima
Cuadrada
27º41' 180 1
Chañaral 29º01' 750 146 6000 1000 788 15 00 2500 2 2021 1, 9, 16
Damas 29º13' 20 20 9, 16
Choros 29º15' 96 32 14 50 720 720 1, 9, 16
Chungungo 29º24’ 400 5
Tilgo 29º32’ 1200 5
Pájaros (1) 29º35' 624 54 880 1000 120 0 1200 1, 9, 16
De los
Huevos
31º55 ' 60 64 274 34 120 1
Papudo 32º30' 100 1
Cachagua 32º35' 1000 1055 2030 2000 1200 1, 14,
16
Concón 32º52' 500 12 100 46 12 10 20 10 1, 16
Pájaro Niño 33º 21' 530 1000 2000 1600 250 1, 16,
18
Papuya 34º00' 14 1
Islot e
Pingüinos
40º56’ 4 3
Puñihuil 41º55' 12 450 50 315 152 1, 13,
14, 15
Metalqui 42º12’ 56 6, 15
humBoldt penguin (SpheniScuS humboldti)
taBle 15.4 Legal actions undertaken by Chile and Peru for the protection of Humboldt penguins in their national
territories
year legal meaSure country deScription reference
1952 DS 797 Chile Bans penguin hunting Iriarte, 1999
1963 DFL RRA 25 Chile Regulates guano trade, banning extraction of guano i n areas with active bird nests
(including those of penguins).
Iriarte, 1999
1966 D S 531 Chile Bans penguin-hunting indenitely. Iriarte, 1999
1967 SM 506 Chile Bans hunting, trans portation, pos session and commercialization of penguins in
Chile.
Iriarte, 1999
1977 RM 01710–77AG-GFFF Peru List s the Humboldt penguin as a Vulnerable species. SPIJ, 2011
1981 DFL 3.557 Chile Allows for extraction of guano in ma rine birds' reproductive sites only w ith Gover n-
mental clearance.
Iriarte, 1999
1993 DS 133 Chile Bans penguin hunting and capturing. Iriarte, 1999
1995 DS 2 25 Chile Implements a 30-year long extract ive ban for marine vertebrates-inc luding Hum-
boldt penguins.
Iriarte, 1999.
1999 DS 013– 99-A G Peru Bans hunting, extraction and expor tation of Humboldt pengui ns for commercial
purposes.
SPIJ, 2011
2004 DS 034–2004-AG Peru Lists the Humboldt penguin as an Endangered Sp ecies and bans its hunting, cap-
turing, p ossession, transportation and exportation for commercial purposes.
SPIJ, 2011
2008 DS 50/2008 Chile Lists the H umboldt penguin as Vulnerable in Ch ile CONAM A, 2010
2009 DS 024–2009-MINAM Peru Implements the gu ano system as a N ational Pr otected Area protec ting most of the
Peruvian breeding sites for the species.
SPIJ, 2011
Note: DFL = Decreto con Fuerza de Ley; DS = Decreto Supremo; RM =Resolución Ministerial
taBle 15.5 Sizes and masses of captive and wild Humboldt penguins’ eggs
location captiVe population-Birdworld great Britain 1wild population-punta San Juan
Year (sample size) 199 0 (n=13) 2002 (n=50)
Measurements Mean ± SD Range Mean ± SD Range
Leng th (cm) 7.200 ± 0.179 6 . 9 97 –7. 4 4 8 7.35 ± 0.33 6. 67 – 8.1 0
Brea dth (cm) 5.559 ± 0. 216 5.056–5.890 5.54 ± 0. 32 4. 8 0 –7.1 0
Initial Mass (g) 122.11 ± 10.81 9 5.18 –13 4 .5 119.28 ± 12.97 84.00–143.00
Sources: Deerling et al., ; Cardeña et al., unpublished data
V. Banded penguinS: genuS SpheniScuS
taBle 15.6 Main constituents of the Humboldt’s diet
location main dietary conStituentS reference
Punta San Juan
15º22’ S
Peruvian anchovy Engraulis ringens Zavalaga an d Paredes 1997b
Silversides Odontesthesregia
Pan de Azucar
26º0 9' S
Garshes Scomberesox saurus Herling et al. (2005)
Peruvian anchovy Engraulis ringens
Jack Macke rel Trachurus murphyi
South American pilchard Sardinops sagax
Chañaral
29º01’ S
Garshes Scomberesox spp. Wilson et al. (1989)
Peruvian anchovy Engraulis ringens
Algarrobo
33º30’ S
Peruvian anchovy Engraulis ringens Wilson et al. (1989)
South American pilchard Sardinops sagax
Puñihuil
45º 55’ S
Peruvian anchovy Engraulis ringens Herling et al. (2005)
Araucanian herring Strangomera bentincki
Silversides Odontesthes regia
Common hake Merluccius gayi
Jack Macke rel Trachurus murphyi
taBle 15.7 Main threats for wild Humboldt populations
reference en gw ep ha p and z Bcf hd hl iaS th
Mur phy (193 6) xx (h) x (h) x (h) xxx
Duf fy (1983) x (h) x (h) x x
Duffy et al. (1984) x (h) x (h) xxxxx
Hays (1984)
Hays (1986) x
Culik and Luna-Jorquera (1997a) x
Battistini (1998)
Paredes and Zavalaga (1998) x
Araya et al. (20 00) xx xxxx
Simeone and Schlatter (1998) x x x x
Simeone et a l. (1999) x
Wallace et al. (1999) x
Culik et al. (20 00) x
Simeone and Bernal (2000) x
Majluf et al. (2 002) x x x
Simeone et a l (2002) x
Taylor et al. (2002) x x X
Cushman (2003) x (h) x (h) xX
Paredes et al. (2003) xx (r) x (r) x (r) xxx
Simeone et a l. 2003 x x X
Herling et al (2005) x
Ellenberg et al. (2006) xX
Boersma et al. (2007) x x
BirdLife International (2008) x x x x x x
Skewgar et al. (20 09) x x X
humBoldt penguin (SpheniScuS humboldti)
Note: reats include EN: El Niño; GW: global warming; EP: Egg poaching; HA: Hunting of adult birds; P and Z: Capturing birds for pets and zoos; B:
By-catch and drowning by net entanglement; CF: Competition with commercial fisheries; HD: Habitat degradation and reproductive failure from Guano
harvests; HL: Loss of nesting sites and reproductive habitat due to coastal development; IAS: Introduction of alien species; TH: Tourism and human
presence. “x” denotes the mentioning or discussing of the threat in the references, (h) stands for historical threat and (r) for recent threat.
referenceS
Araya, B., D. Garland, G. Espinoza, A. Sanhuesa, A . Simeone, A. Teare, C.
Zavalaga, R. Lacy, and S. Ellis, eds. . Population and habitat viabil-
ity analysis for the Humboldt penguin (Spheniscus humboldti). Final
report. Apple Valley, MN: IUCN/SSC Conservation Breeding Specialist
Group.
Araya, B., and F. S. Todd. . Status of the Humboldt penguin in Chile
following the – El Niño. Proceedings of the Jean Delacour/IFCB
Symposium, Los Angeles, –.
Baker, A. J., S. L. Pereira, O. P. Haddrath, and K. A . Edge. . Multiple
gene evidence for expansion of extant penguins out of Antarctica due to
global cooling. Proceedings of the Royal Society B :–.
Battistini, G. . El nido del pingüino de Humboldt (Spheniscus hum-
boldti) y su relación con el éxito reproductivo. Tesis para optar el título
Licenciado en Biología, Universidad Peruana Cayetano Heredia, Lima,
Perú.
Battistini, G., and R. Paredes. . Nesting habits and nest characteristics
of Humboldt penguins at Punta San Juan, Peru. Penguin Conservation
:–.
Bertelli, S., and N. P. Giannini. . A phylogeny of extant penguins
(Aves: Sphenisciformes) combining morphology and mitochondrial
sequences. Cladistics, :–.
Bertrand, A., F. Gerlotto, S. Bertrand, M. Gutierrez, L. Alza, A. Chipol-
lini, E. Diaz, P. Espinoza, J. Ledesma, R. Quesquen, S. Peraltilla, and
F. Chavez. a. Schooling behaviour and environmental forcing in
relation to anchoveta distribution: An analysis across multiple spatial
scales. Progress in Oceanography :–.
Bertrand, S., B. Dewitte, J. Tam, E. Díaz, and A. Bertrand. b. Impacts
of Kelvin wave forcing in the Peru Humboldt Current system: Scenarios
of spatial reorganizations from physics to fishers. Progress in Oceanog-
raphy :–.
BirdLife International . BirdLife International/American Bird Con-
servancy Workshop on Seabirds and Seabird-Fishery Interactions in
Peru. RSPB (Royal Society for the Protection of Birds), Sandy, United
Kingdom.
Boersma, P. D. . Breeding patterns of Galápagos penguins as an indica-
tor of oceanographic conditions.Science :–.
———. . Population trends of the Galápagos penguin: Impacts of El
Niño and La Niña. Condor :–.
———. . Penguins as marine sentinels. BioSicence ():–.
Boersma, P. D., S. Branch, D. Butler, S. Ellis-Joseph, P. Garland, P. McGill, G.
Phipps, U. Seal, and P. Stockdale. . Penguin Conservation Assess-
ment and Management Plan. Apple Valley, MN: IUCN/SSC Captive
Breeding Specialist Group.
Boersma, P. D., G. A. Rebstock, D. L. Stokes, and P. Majluf. . Oceans
apart: Conservation models for two temperate penguin species shaped
by the marine environment. Marine Ecology Progress Series :–.
Boersma, P. D., and D. L. Stokes. . Conservation of penguins: reats to
penguin populations. In Bird Families of the World: e Penguins, ed. T.
D. Williams, –. Oxford: Oxford University Press.
Christensen, V., and C. J. Walters. . Ecopath with Ecosim: Methods,
capabilities and limitations. Ecological Modelling :–.
Coffin, H. R., J. V. Watters, and J. M. Mateo. . Odor-based recognition
of familiar and related conspecifics: A first test conducted on captive
Humboldt penguins (Spheniscus humboldti). PLoS ONE ():e.
Coker, R. E. . Habits and economic relations of the guano birds of Peru.
Proceedings of the United States National Museum :–.
CONAMA (Comisión Nacional del Medio Ambiente). . Decreto
Supremo No. /. http://www.conama.cl/clasificacionespecies/
Anexos_segundo_proceso/DS___doProcesoClasif_completo.
pdf.
Culik, B., J. Hennicke, and T. Martin. . Humboldt penguins outma-
noeuvring El Niño. Journal of Experimental Biology :–.
Culik, B. M., and G. Luna-Jorquera. a. Satellite tracking of Humboldt
penguins (Spheniscus humboldti) in northern Chile. Marine Biology
:–.
———. b. e Humboldt penguin Spheniscus humboldti: A migratory
bird? Journal of Ornithology :–.
Culik, B. M., G. Luna-Jorquera, H. Oyarzo, and H. Corre a. . Humboldt
penguins monitored via VHF telemetry. Marine Ecology Progress Series
:–.
Cursach, J., J. Vilugrón, C. Tobar, J. Ojeda, J. Rau, C. Oyarzún, and O. Soto.
. Nuevos sitios de nidificación para cuatro especies de aves mari-
nas en la provincia de Osorno, centro-sur de Chile. Boletín Chileno de
Ornitología :–.
Cury, P., A. Bakun, R. J. M. Crawford, A. Jarre, R. A. Quiñones, L. J. Shan-
non, and H. M. Verheye. . Small pelagics in upwelling systems: Pat-
terns of interaction and structural changes in “wasp-waist” ecosystems.
ICES Journal of Marine Science :–.
Cury, P. M., L. J. Shannon, J. P. Roux, G. M. Daskalov, A. Jarre, C. L.
Moloney, and D. Pauly. . Trophodynamic indicators for an ecosys-
tem approach to fisheries. ICES Journal of Marine Science :–.
Cushman, G. T. . e lords of guano: Science and the management of
Peru’s marine environment, –. PhD diss., University of Texas
at Austin.
Deeming, D. C., R. L. Harvey, L. Harvey, S. Carey, and D. Leuchars. .
Artificial incubation and hand rearing of Humboldt penguins (Sphe-
niscus humboldti) at Birdworld, Franham. International Zoo Yearbook
:–.
Duffy, D. C. . e foraging ecology of Peruvian seabirds. e Auk
():–.
Duffy, D. C., C. Hays, and M. A. Plengue. . e conservation status
of Peruvian seabirds. In Status and Conservation of the World’s Sea-
birds, ed. J. P. Croxall, P. G. H. Evans , and R. W. Schreiber, –. ICBP
Technical Publication No. . Cambridge: International Council for Bird
Preservation.
Ellenberg, U., T. Mattern, P. J. Seddon, and G. Luna-Jorquera. .
Physiological and reproductive consequences of human disturbance in
Humboldt penguins: e need for species -specific visitor management.
Biological Conservation :–.
Garcia, S. M., A. Zerbi, C. Aiaume, T. Do Chi, and G. Lasserre. . e
ecosystem approach to fisheries: Issues, terminology, principles, insti-
tutional foundations, implementation and outlook. Food and Agricul-
taBle 15.7 (Cont.)
V. Banded penguinS: genuS SpheniScuS
tural Organization Fisheries Technical Paper No. . Rome: Food and
Agricultural Organization.
Guevara-Carrasco, R., M. Niquen, and M. Bouchon. . A summary
on monitoring, assessment and criteria to estimate the total allowable
catch of the Peruvian anchoveta (northern-central stock). Document
submitted by the Instituto del Mar del Perú (IMARPE) at the Lenfest
Forage Fish Task Force Meeting, Paracas , Peru.
Hays, C. . e Humboldt penguin (Spheniscus humboldti) in Peru and
the effects of the – El Niño. MSc thesis, University of Florida.
——— . Effects of the El Niño – on Humboldt penguin colonies
in Perú. Biological Conservation :–.
Hennicke, J. C., and B. M. Culik. . Foraging performance and repro-
ductive success of Humboldt penguins in relation to prey availability.
Marine Ecology Progress Series :–.
Herling, C., B. M. Culik, and J. C. Hennicke. . Diet of the Humboldt
penguin (Spheniscus humboldti) in northern and southern Chile.
Marine Biology :–.
Hertel, F., D. Martinez, M. Lemus, and J. C. Torres-Mura. . Birds from
Chungungo, Tilgo, and Pájaros Islands in north-central Chile. Journal
of Field Ornithology (): –.
Hiriart-Bertrand, L., A. Simeone, R . Reyes-Arriagada, V. Riquelme, K.
Pütz, and B. Lüthi. . Descripción de una colonia mixta de pingüino
de Humboldt (Spheniscus humboldti) y de Magallanes (S. magellanicus)
en Isla Metalqui, Chiloé, sur de Chile. Boletín Chileno de Ornitología
:–.
Iriarte, A. . Marco legal relativo a la conservación y usosustentable de
aves, mamíferos y reptiles en Chile. Estudios Oceanológicos :–.
IUCN (International Union for Conservation of Nature). . IUCN red
list of threatened species. Version . http://www.iucnredlist.org.
Jahncke, J., D. M. Checkley, and G. L. Hunt. . Trends in carbon flux of
seabirds in the Peruvian upwelling system: Effects of wind and fisheries
on population regulation. Fisheries Oceanography ():–.
Ksepka, D. T., S. Bertelli, and N. P. Giannini. . e phylogeny of living
and fossil Sphenisciformes (penguins). Cladistics :–.
Luna-Jorquera, G., and M. Cortes. . Estudio del ensamble de aves y
mamíferos marinos al interior del Área Marina y Costera Protegida de
Múltiples Usos Isla Grande de Atacama. In Conservación de la Biodi-
versidad de Importancia Mundial a lo largo de la Costa Chilena. Gobi-
erno de Chile.
Luna-Jorquera, G., and B. M. Culik. . Penguins bled by vampires. Jour-
nal of Ornithology :–.
———. . Diving behaviour of Humboldt penguins Spheniscus hum-
boldti in northern Chile. Marine Ornithology :–.
———. . Metabolic rates of swimming Humboldt penguins. Marine
Ecology Progress Series :–.
Luna-Jorquera, G., S. Garthe, F. G. Sepulveda, T. Weichler, and J. A.
Vásquez. . Population size of Humboldt penguins assessed by
combined terrestrial and at-sea counts. Waterbirds: e International
Journal of Waterbird Biology ():–.
Majluf, P., E. A. Babcock, J. C. Riveros, M. Arias-Schreiber, and W. Alde-
rete. . Catch and by-catch of sea birds and marine mammals in
the small-scale fishery of Punta San Juan, Peru. Conservation Biology
():–.
Martin, G. R., and S. R. Young. . e eye of the Humboldt penguin,
Spheniscus humboldti: Visual fields and schematic optics. Proceedings
of the Royal Society of London B :–.
Mattern, T., U. Ellenb erg, G. Luna-Jorquera, and L. Davis . . Humboldt
penguin census in Isla Chañaral, Chile: Recent increase or past under-
estimate of penguin numbers? Waterbirds: e International Journal of
Waterbird Biology ():–.
Melly, P., J. Alfaro-Shigueto, J. Mangel, M. Pajuelo, C. M. Cáceres, L. San-
tillán-Corrales, D. Montes-Iturrizaga, K. Baella, and J. Janhcke. .
Assessment of seabird by-catch in Peruvian artisanal fisheries. Final
report to the British Petroleum Conservation Programme. Pro Delphi-
nus, Lima.
Ministerio del Ambiente. . Servicio Nacional de Áreas Naturales
Protegidas por el Estado. www.sernanp.gob.pe/sernanp/bmapas.
jsp?NroPag=andID= (accessed April ).
Murphy, R. C. . Oceanic Birds of South America. Vol. . New York:
American Museum of Natural History.
Olsen, S. B., G. G. Page, and E. Ochoa. . e analysis of governance
responses to ecosystem change: A handbook for assembling a base-
line. LOICZ Reports and Studies No. . Geesthacht, Germany: GKSS
Research Center. pp.
Otsuka, R., T. Machida, and M. Wada. . Hormonal correlations
at transition from reproduction to molting in an annual life cycle of
Humboldt penguins (Spheniscus humboldti). General and Comparative
Endocrinology :–.
Paredes, R., and C. B. Zavalaga. . Overview of the effects of El Niño
– on Humboldt penguins and other seabirds at Punta San Juan,
Perú. Penguin Conservation :–.
———. . Nesting sites and nest types as important factors for the con-
servation of Humboldt penguins (Spheniscus humboldti). Biological
Conservation :–.
Paredes, R., C. B. Zavalaga, G. Battistini, P. Majluf, and P. McGill. .
Status of the Humboldt penguin in Peru, –. Waterbirds: e
International Journal of Waterbird Biology ():–.
Paredes, R., C. B. Zavalaga, and D. J. Boness. . Patterns of egg laying
and breeding success in Humboldt penguins (Spheniscus humboldti) at
Punta San Juan. e Auk ():–.
Pauly, D., V. Christensen, J. Dalsgaard, R. Froese, and F. C. Torres. .
Fishing down marine food webs. Science :–.
Pauly, D., and M. L. Palomares. . Fishing down marine food web: It
is far more pervasive than we thought. Bulletin of Marine Science
():–.
Pizarro, C. A. . Áreas marinas protegidas y usutilidad en la conserva-
ción de las aves marinas en Chile. Tesis de pregrado, Facultad de Cien-
cias, Universidad de Chile.
Schlosser, J. A., J. M. Dubach, T. W. J. Garner, B. Araya, M. Bernal, A. Sime-
one, K. A. Smith, and R. S. Wallace. . Evidence for gene flow dif-
fers from observed dispersal patterns in Humboldt penguin, Spheniscus
humboldti. Conservation Genetics :–.
Scholten, C. J. . Breeding biology of the Humboldt penguin (Spheniscus
humboldti) at Emmen Zoo. International Zoo Yearbook :–.
———. . Iris colour of Humboldt penguins Spheniscus humboldti.
Marine Ornithology :–.
Schwartz, M. K., D. J. Boness, C. M. Schaeff, P. Majluf, E. A. Perry, and
R. C. Fleischer. . Female-solicited extrapair matings in Humboldt
penguins fail to produce extrapair fertilizations. Behavioral Ecology
():–.
Simeone, A. . Evaluación de la población reproductiva del pingüino de
Magallanes y del pingüino de Humboldt en los islotes Puñihuil, Chiloé.
Informe final. Estudio financiadopor la Fundación Otway (Chile) y Zoo
Landau in der Pfalz (Alemania). Viña del Mar. pp.
Simeone, A., B. Araya, M. Bernal, E. N. Diebold, K. Grzybowski, M.
Michaels, J. A. Tare, R. C. Wallace, and M. J. Willis. . Oceano-
graphic and climatic factors influencing breeding and colony atten-
dance patterns of Humboldt penguins Spheniscus humboldti. Marine
Ecology Progress Series :–.
Simeone, A., and M. Bernal. . Effects of habitat modification on
breeding seabirds: A case study in central Chile. Waterbirds: e Inter-
national Journal of Waterbird Biology ():–.
Simeone, A., M. Bernal, and J. Meza. . Incidental mortality of Hum-
boldt penguins Spheniscus humboldti in gill nets, central Chile. Marine
humBoldt penguin (SpheniScuS humboldti)
Ornithology :–.
Simeone, A., L. Hiriart-Bertrand, R . Reyes-Arriagada, M. Halpern, J.
Dubach, R. Wallace, K. Pütz, and B. Lüthi. . Heterospecific pairing
and hybridization between wild Humboldt and Magellanic penguins in
southern Chile. Condor ():–.
Simeone, A., G. Luna-Jorquera, M. Bernal, S. Garthe, F. Sepúlveda, R.
Villablanca, U. Ellenberg, M. Contreras, J. Muñoz, and T. Ponce. .
Breeding distribution and abundance of seabirds on islands off north-
central Chile. Revista Chilena de Historia Natural :–.
Simeone, A., and R. P. Schlatter. . reats to a mixed-species colony of
Spheniscus penguins in southern Chile. Colonial Waterbirds ():–
.
Skewgar, E., A. Simeone, and P. D. Boersma. . Marine reserve in Chile
would benefit penguins and ecotourism. Ocean and Coastal Manage-
ment :–.
Smith, K. M., W. B. Karesh, P. Majluf, R. Paredes, C. Zavalaga, A. Hoo-
gesteijn-Reul, M. Stetter, W. E. Braselton, H. Puche, and R. A. Cook.
. Health evaluation of free-ranging Humboldt penguins (Sphenis-
cus humboldti) in Peru. Avian Diseases :–.
SPIJ (Sistema Peruano de Información Jurídica). . Sistema Peruano de
Información Jurídica. http://spij.minjus.gob.pe.
Taylor, S. S., M. L. Leonard, D. J. Boness, and P. Majluf. . Foraging by
Humboldt penguins (Spheniscus humboldti) during the chick-rearing
period: General patterns, sex differences, and recommendations to
reduce incidental catches in fishing nets. Canadian Journal of Zoology
:–.
———. . Humboldt penguins Spheniscus humboldti change their
foraging behaviour following breeding failure. Marine Ornithology
:–.
Teare, J. A., E. N. Diebold, K. Grzybowski, M. G. Michaels, R. S. Wallace,
and M. J. Willis. . Nest site fidelity in Humboldt penguins (Sphe-
niscus humboldti) at Algarrobo, Chile. Penguin Conservation :–.
iel, M., E. C. Macaya, E. Acuña, W. E. Arntz, H. Bastias, K. Brokordt,
P. A. Camus, J. C. Castilla, L. R. Castro, M. Cortés, C. P. Dumont, R.
Escribano, M. Fernandez, J. A. Gajardo, C. F. Gaymer, I. Gomez, A. E.
Gonzales, H. E. Gonzalez, P. A. Haye, J. E. Illanes, J. L. Iriarte, D. A.
Lancellotti, G. Luna-Jorquera, C. Luzoro, P. H. Manriquez, V. Marín, P.
Muñoz, S. A. Navarrete, E. Perez, E. Poulin, J. Sellanes, H. Sepúlveda,
W. Stotz, F. Tala, A. omas, C. A. Vargas, J. A. Vasquez, and J. M.
A. Vega. . e Humboldt Current System of northern and central
Chile: Oceanographic processes, ecological interactions and socioeco-
nomic feedback. Oceanography and Marine Biology: An Annual Review
:–
UNEP (United Nations Environment Programme). . World Conserva-
tion Monitoring Centre report on the status and conservation of the
Humboldt penguin Spheniscus humboldti. United Nations Environ-
ment Programme World Conservation Monitoring Centre, Cambridge.
Van Buren, A. N., and P. D. Boersma. . Humboldt penguins (Sphe-
niscus humboldti) in the Northern Hemisphere. e Wilson Journal of
Ornithology ():–.
Vargas, F. H., S. Harrison, S. Rea, and D. W. Macdonald. . Biological
effects of El Niño on the Galápagos penguin. Biological Conser vation
:–.
Wallace, R. S., J. Dubach, M. G. Michaels, N. S. Keuler, E. D. Diebold, K.
Grzybowski, J. A. Teare, and M. J. Willis. . Morphometric determi-
nation of gender in adult Humboldt penguins (Spheniscus humboldti).
Waterbirds ():–.
Wallace, R. S., K. Grzybowski, E. Diebold, M. G. Michaels, J. A. Teare, and
M. J. Wills. . Movements of Humboldt penguins from a breeding
colony in Chile. Waterbirds: e International Journal of Waterbird
Biology ():–.
Ward, T., D. Tarte, E. Hegerl, and K. Short. . Policy proposals and
operational guidance for ecosystem-based management of marine cap-
ture fisheries. World Wide Fund for Nature, Australia.
Williams, T. D. . e Penguins. Oxford: Oxford University Press.
Wilson, R. P., D. C. Duffy, M. P. Wilson, and B. Araya. . e ecology of
species replacement of Humboldt and Magellanic penguins in Chile. Le
Gerfaut :–.
Wilson, R. P., M. P. Wilson, D. C. Duffy, B. M. Araya, and N. Klages. .
Diving behavior and prey of Humboldt penguin (Spheniscus hum-
boldti). Journal of Ornithology :–.
Zavalaga, C. B., and R. Paredes. a. Sex determination of adult Hum-
boldt penguins using morphometric characters. Journal of Field Orni-
thology ():–.
———. b. Humboldt penguins in Punta San Juan, Peru. Penguin Con-
servation ():–.
