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Are the Adélie penguin, Pygoscelis adeliae, populations with breeding
colonies in the Ross Sea being affected by the establishment of the Ross Sea
region Marine Protected Area?
Elizabeth Howarth
University of North Carolina, Wilmington
BIO 484: Research Methods in Biology
Dr. Troy Alphin
November 30, 2021
Rational:
The focusonthisstudyistoevaluate how the populationsizeandhealthof Adélie penguin,Pygoscelis
adeliae, colonies at Cape Royds, Cape Bird and Cape Crozier have changed over time, especially in
relation to the Ross Sea region Marine Protected Area, MPA, established in 2017 and considering
major environmental and biological factors that could have an effect on these populations. We will
continue tocollectnewdataannually tolookatanyaffectstheRossSearegionMPA ishavingonthese
populations. Using data about population sizes of coloniesand health of individuals from within the
colonies,wewillevaluatethe overallhealthofthe colonies andpredicthowwe expectthemtochange
in the near future. This is an important study as P. adeliae are an indicator species for their local
ecosystem – the health of the penguin colonies reflects the health of the local ecosystem.
Introduction:
Marine Protected Areas, MPAs:
MPAs involve the spatial zoning of a marine environment for either the conservation of: individual
species, habitats or whole ecosystems through the regulation human activity within that area
(Hoagland et al., 2019) and are focused in areas that are most vulnerable to natural and artificial
disturbances (Australian Association for Maritime Affairs, 2012). Classifications of MPAs involve
definingthe protectedareaasasimple andaccurate reflection of the proposedgoalsandapproaches
(designed specifically for that individual area) as well as allowing assessmentsof associatedimpacts
the MPA couldpresent,whilsthavingminimalimplications(NOAA,n.d.).The effectivenessof anMPA
is presented by the unique balance of intensity of exploitation, type of management programmes
implemented, and overall protection implemented in the area (WCPA, 2018). Previous studies have
shownthatthe most effective MPAs all have 5keyfeatures:MPA setasa no-take zone, implemented
lawsare well enforced,the MPA is establishedfor more than 10 years, it is an area greater than 100
km2
, and the zone is isolated by either deep water or sediment (Edgar, 2014).
Antarctica and it’s corresponding waters contain many endemic and well adapted species, so it’s
important that as environmental conditions begin to change (due to natural and anthropogenic-
induced disturbances) we must begin to design and enforce protection projects within the most
vulnerable areas to limitany disturbances to the local terrestrial and marine ecosystems(Kavanagh,
2020). It has also been suggestedthat is all MPAs, proposed and currentlyenforced, in and around
Antarctica were accepted as a permanentfeature then a positive impactonmany specieswouldbe
observed; some species could also show significant increase in population size (University of East
Anglia, 2021).
Figure 1 – proposed and existing MPAs in the Southern Ocean, surrounding Antarctica – The map shoes how the Southern
Ocean is separated into 9 different domains and also shows existing continental MPAs, MPAs protecting subantarctic
islands and Proposed MPAs which will protect more of the coast of the Antarctic continent (PEW Charitable Trust, 2019)
The Ross Sea region MPA, which became established in December 2017 by Commission for the
Conservation of Antarctic Marine Living Resources (CCAMLR) – for at least 35 years – (Dodds, 2018)
includes the Ross Sea Continental Shelf, which is one of the most productive areas of the Southern
Ocean.AsSeeninfigure 1,the RossSearegionMPA isfoundwithindomain8andcoversanextensive
area; in fact, it is the world’s largest MPA at 2.09 million km2
.
Figure 2 – map of Ross Sea region MPA – this map clearly shows the distribution of the different types of zones within this
MPA region. (Crown, 2016)
ThisMPA has3 differentlevelstypesof zoneswithinit,whichinclude:General ProtectionZones(GPZ),
Special ResearchZones(SRZ) and Krill ResearchZones(KRZ) (Crown, 2016). The distributionof these
3 zones are shown in figure 2. GPZ covers the most heavily protected areas where no fishing is
permitted, SRZ allow limited fishing of krill and toothfish for research only and KRZ is slightly more
relaxed by allowing controlled krill fishing but still only for research (Marine Conservation Institute,
2021).
Adélie Penguins, Pygoscelis adeliae:
P. adeliae breed on and around the continent and consume mostly krill and other oceanic prey for
food – because of this they are a good indicator species for the marine ecosystem.Previous studies
that tracked P. adeliae showed they can travel thousands of kilometres during winter to feed and
returnto the same colonies atthe start of theirbreedingseason(Conveyetal.,2013). Theirbreeding
seasonbeginsinOctoberandaverage colonypeakegglayingismid-November,whichgivesthe chicks
time to grow before they have to fledge their colonies by March (Barreau, 2019).
Parent penguins have to use a lot of metabolic energy to raise their chicks – both parents have to
spendmanyweeksfastingtolookafterthe eggornewlyhatched chick.Theytake turnstogoforaging
forfood,where theyhave tocollectenoughfoodforthemandtheirchick (aschickiscurrentlyunable
to swimor hunt for own food). Predation andphysiological limitsare majorbioticfactors that affect
the magnitude of parental care giventothe chicks(Chappell,1993).Abioticfactorssuchastime limits
and sea ice concentration may also affect foraging and breeding successes; negative correlation
between increased sea ice and breeding/foraging successes have been identified. Increased ice has
been associated with colder temperatures, meaning individuals must use more metabolic energy
keepingwarmthanif it was a warmer year.Also increased seaice meansparentsmusttravel further
to openwaterthaninotheryears –thisnotonlyincreasesforagingtrips,butalso meansparentsmust
catch more food, as they require more energy to make that journey, but must still have enough to
feed their chicks (Barreau, 2019).
Phenological timing of the beginning of the breeding season is driven by a combination of
physiological, ecological and behavioural processes as well as environmental cues prior to the
breeding season. A previous study conducted at Bechervaise Island, East Antarctica showed that P.
adeliae respond to changes in environmental conditions by adjusting their timings of breeding –
demographic consequences less well understood. The changing environmental conditions directly
impactthe penguinsbyimpactingforagingandcolonyaccessibility.Ithasbeensuggestedthat further,
more pronounces environmental and phenological changes could have problematic effects on
breeding populations (Emmerson, 2011).
Collection of organic matter from P. adeliae at multiple abandoned colonies have beendated, using
radiocarbondating, andshowthatthe therehasbeenalonghistoryof colonisationandabandonment
throughout the Ross Sea region. The oldest samples so far have dated back to 45 000 years ago.
Radiocarbon dates of multiple samples of bone, tissue and eggshell of P. adeliae confirm that the
oldestcolonieswere presentfrom45 000 – 27 000 yearsbefore present(yrB.P.).There wasthen an
abandonmentperioduntil8000 yr B.P. – due tothe lastadvancementof the RossIce Sheet.Between
thenand presentday,there have been 2 further periods of abandonment (5 000 – 4 000 and 2 000 –
1 100 yr B.P.) that correlate to cooling periods which had unfavourable marine conditions. Finally,
datingsuggestsmost moderncolonieshave all beenestablishedwithinthe past2 000 years(Emslie,
2007)
Working in Antarctica:
Antarcticaisa verychallengingenvironmenttoworkinandrequires alotof preparationandplanning
fromeveryone onthe team –some of the majorchallenges scientistsface whenworkinginAntarctica
include: challenging weather, accessibility (to research stations and to field sites), technology and
equipment failure, safety and composition of the team (Sanson, 2013).
Before stepping foot in Antarctica, preparation of individual members of the team and preparation
for the actual science proposed tohappenmustoccur. Everymemberof the team mustundergopre-
deploymenttrainingand medical testing,aswell asreceivingtheirkit,includingappropriate clothing
for the environment– this ensures the safety of the team throughout their time in Antarctica and
allows each team member to become familiar with how life in Antarctica is different to outside
Antarctica, as well as how the research station and field sites work (National Science Foundation,
2018). AsRoss Islandis an Antarctic SpeciallyProtectedArea(ASPA) –designatedbythe Protocol on
Environmental Protection to the Antarctic Treaty - a permit is required to enter and work in those
areas.The permitsare allocatedby the National Science Foundation(NSF).The NSF isalsothe largest
granting body within the USA, a grant is also required to work within Antarctica. (Rejcek, 2008)
Wheninthe field,weathercanbe unpredictableanddangerous,ascanchange frommildto severe in
the space of minutes. The use of training, completion of risk assessments and availabilityof survival
bags when off base, all of these increase chance of survival if natural disasters, cold climates or
extreme weatherwastooccurwheninthe field.Whilstinthe fieldalso,allequipment,transportation,
food, and other things usually needed for the logistics of the field research are provided by the
granting body, the trade-off being there is some part of your schedule that you can’t control; for
example youcanonlygotodo yourfieldworkaslongasthere isroomat the local researchstation for
when you are not in the field. (Vervoort, 2011)
Objectives:
 Compare P. adeliae populationgrowthsof colonies from1983 – presentandinto the future.
To do this I will:
o Use past collected data of aerial counts of population size for each colony at each
study site
o Conductnew aerial andground populationsize countsforeach colonyat each study
site
o Collectdatatocalculate how manychicksare beingraisedpercolonyperyear ateach
study site
 Evaluate health of the penguin colonies. To do this I will:
o Measure height, weight and sex of individual adults as soon as the exit the water at
the beginning of the breeding season at each study site
o Measure weightof chicksjustbefore theyenterthe water,astheyfledge the colony,
at the end of the breeding season at each study site
 Evaluate how colony population sizes have changed over time:
o See if the MPA establishment has had any effect of the colonies
o Evaluate how the health of the colonies and individuals within the colonies are
changing
o compare datafromdifferentyearsandalsoevaluate ifonecolonyismore healthy/has
more healthy individuals than another colony
o Predict how the population sizes may change in the near future
o This evaluation will include constructing graphs and completing statistical tests
Methods:
Study Sites:
Figure 3 - This map of Ross Island, this island can be shown in respect to the Antarctic continent in the small diagram of
Antarctica in the left, bottom corner. On the Island, the 3 labels show the location of the 3 different colonies I’m going to
look at throughout my experiment. These colonies are at Cape Royds (indicated by yellow dot), Cape Bird (indicated by
purple dot) and Cape Crozier (indicated by pink dot). (Mike, 2013)
Figure 3, showingRossIsland and the 3 P. adeliae colonysitesI’ve chosen to use for my study.Cape
Royds represents smaller colonies, Cape Bird represents medium sized colonies and Cape Crozier
represents larger colonies.As well as representing a wide size range of colonies, all 3 sites have had
data collected consecutivelyoverthe pastfew decades,meaningall 3sitesare representable for the
studyand allowmaximumreliabilityof the analysiswe will be completingwithinthisstudy. Ontopof
this,eachlocationhasitsown slightlydifferentweatherconditionsandchallenges,makingthe results
further representative of the whole Ross Sea region.
Data Collection:
The aerial countsof populationsizescollectedinpreviousyearsare sourcedfromthe Adélie Penguin
Census,whichisprovidedbyAntarcticaNew Zealand –agovernmental agencythatisresponsiblefor
science and environmental protection activities that New Zealand complete within Antarctica
(Antarctica New Zealand, 2021)
All data collected as a part of this study will be within the guidelines provided in the CCAMLR
Ecosystem Monitoring Programme (CEMP) Standard Methods handbook. These standard methods
were establishedtoregulate the methodof datacollection;asall data collectedmustbe sharedwith
CCAMLR, it allows the formation of standardised data series which are freely accessible (CCAMLR,
2014)
Firstly,inregardtocollectingdatatohelpme analysethe healthof the colonybylookingatindividuals
withinthe colonies,Iwill collectdataof adultsastheyarrive at the breedingsitethe beginningof the
breedingseasonanddataonchicksastheyfledgethe breedingsiteatthe endof the breedingseason.
Whencollectingthe weight,sex andheightof adult penguins,astheyarrive ontobeachof theircolony,
I will followStandardMethodA1(v3). Whencollectingthe weightof chicksasthey fledgetheircolony
via the beach, I will follow Standard Method A7 (v4) procedure A.
Secondly,inregardtocollectingdatatocontinuemonitoringthe populationsizes ateachcolony,Iwill
complete aerial counts, using UnmannedAerial Vehicle (UAV) drones, and ground counts,as well as
calculatingthe numberof chicksraisedpercolony.Toconductgroundpopulationcounts,Iwill follow
StandardMethodA3A (v4). Whilstconductingaerial populationcounts,Iwill followStandardMethod
A3B (v1). Whist collecting data about breeding success (which will be used when calculating chicks
raised per colony), I will follow Standard Method A6 (v5) Procedure C.
All methods are explained in detail in CCAMLR Ecosystem Monitoring Program Standard Methods
handbook, revised in June 2014.
Data Representation and Analysis:
Populationsizesatall 3sitesare andwill be representedinasimplelinegraph. Plottingall mydataon
only1 setof axisallowsforeasieridentificationof anypatternsoccurringatthe same timeatdifferent
colony sites.Italsoallows foran overall trendstobe observed. We decidedtoadda secondaryx-axis
forCape Royds,so the trendof all 3 sitescanbe easilyobserved,onlyhavingasingle x-axismeantthe
trends of Cape Royds couldn’t be observed well.
Statistical T-tests, using mean population sizes for pre- and post- MPA establishment could also be
helpful – this will me more accurate as collect more data as currently only have 2 data points, per
colonysite.T-testscouldalsocompare groundpopulationsizecountsandaerial populationsize counts
from the same year to identify if there is any significant differences between the 2 methods of
collecting the same data. A previous study with a simulated colony set-up suggests that population
sizes collected from Unmanned Aerial Vehicles (UAV), compared to ground-based counts,are more
accurate (Hodgson, 2018).
To evaluate breeding success, we will compare the number of eggs laid to the number of chicks
fledging.Thiswill allowustocalculate the successrate of parentingperyearat eachcolony,withthis
data we can compare parental successrates betweencoloniesand view the trendof how successful
breeding at a single colony is from year to year.
The constructionof a populationmodel,fromthe datawe will collectcanallow usandotherscientist
to studythe populationdynamicsof eachcolonysite.The modelcouldthenbe appliedwithdifferent
parameters to estimate how the population is expected to change in the near future with those set
parameters.
Results:
Analysisof Past Data:
As previously stated, this data is from the Adélie Penguin Census and shows aerial population size
counts from the early 1980s to present day – unfortunatelydue to COVID-19, no data was collected
inyears2019 and2020, meaningthere willbe atleasta2-yeargapinmyaerial populationsizedataset.
Hopefullyas we get more data over the next few years, we can make accurate estimations on what
the data probably would have shown if data was collected in those years.
Figure 4 - – aerial survey data from 1983 – 2018 based on data from Adélie Penguin Census, Antarctica New Zealand, for
Cape Royds, Cape Bird and Cape Crozier. In the Census, Cape Bird was split into North, Middle and South and Cape Crozier
was split into West and East – in this graph I have combined them to get total counts for each colony area. There was no
count collected: Cape Bird North 2000, Cape Bird Middle 2008 and Cape Crozier West 2000. No data collected for these
times can explain the abnormalities for these years within my graph (Cape Bird 2000 and 2008 and Cape Crozier 2000).
Previouslycollected data,representedinfigure 4, showsmildannual variety duetovariationincensus
dates, weather and climatic differences throughout the years and differing sea ice content
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Cape Bird Cape Crozier Cape Royds
surroundingthe breedingsites(Taylor,1990).Previouscomparisonsof the Adélie PenguinCensuswith
local climatic events occurring at the same time have shown that generally,years with increased
temperaturesinthe Ross Sea regionhave positivelyinfluenced P.adeliae populationsinthose years
– thismay be due toeasieraccesstoopenwater, increasedlocalproductivityof the RossSea(causing
increased food availability), lower winter mortality,enhanced breeding success or a combination of
these factors (Taylor, 1990). All colonies, especially Cape Royds and Cape Crozier were drastically
affectedbythe icebergs in2000/2001 that changedthe local environmentaroundthe colonysites, in
those years.These icebergshadanegative impactonthe coloniesbreedingatthose sites andcaused
decreased successful reproduction and decreased survival rates in the years the icebergs were
present.
Cape Royds:
In 2000, multiple large icebergs broke off the Ross Ice Shelf and caused lots of sea ice to build up,
become stuckand unable to melt.Thiswas a disadvantage tothe Cape Roydscolonyand because of
thisin2000 lesschickswere produced –probablymostlyduetothe increasedenergyneededtoaccess
openwaterduring the breedingseasontoforage for foodfor themselvesandtheirchicks.Aswell as
this, many breeding pairs moved from Cape Royds to other local breeding sites, including Cape Bird
and Beaufort Island. Luckily, over the next few years as the sea ice broke up, the colony recovered,
and the population size of the colony increased again (Rejcek, 2008).
Since 2000, the population at Cape Royds has remained to increase and in the next few years could
be expectedtobe backatthe same approximate size asitwasbeforethe devastatingincidentin2000.
Thisproveshowdelicate these populationsare tochangesintheirenvironment andfurthersupports
whyitissoimportanttoprotecttheirlocal environments;ithastakenthiscolony>15yearstorecover,
and is still recovering, however many colonies that face disaster end up becoming completely
abandoned and separated to multiple other local colonies.
Cape Crozier:
Cape Crozier, the largest colony in my study, has previously been thought to be a self-regulating
population andbecause of this,unlikelytocollapse because of populationpressure –ithas alsobeen
suggestedthatmore extreme weatherandanthropogenicimpactsare likelytoaffectthispopulation
inthe future (Rejcek,2008). Asa largercolony,individualsthatbreedatthissite are requiredtospend
more energy to collect food during foraging trips, this is due to increased intraspecific competition
between individualswithin this population. Duration of the foraging trips and metabolic rates are
likely to be increased compared to the other 2 colonies within this study (Balance, 2009).
During1980’s and 1990’s there wasa slightdeclineinpopulationsize.Due tosome missingdatafrom
Cape Crozier in the year 2000, it is unknown exactly when the sudden decrease in population size
occurred. However the arrival of giant icebergs, B15A and C16, in the Ross Sea in January 2001
(Kooyman,2007), can explainthe decrease of >89 000 individuals between the years 1999 and 2001.
Since then, the population has drastically increased,on average, with 2018’s data showing a colony
size of over 300 000 individuals – up from approximately 67 000 individuals in 2001.
Cape Bird:
Cape Bird,the most northernsite withinthisstudy,sits at the tip of Ross Island.The populationsize
of the colony at this site has remained fairlyconstant from 1983-2018 (the years we have data for),
showing no major variations in population size. This is probably due to the fact this site hasn’t been
affected by any major weather disturbances or anthropogenic disturbances that would affect
reproductionrates or survival rates.It has beensuggestedthatfood may be limited,partiallydue to
environmental stochasticity, and this could explain why the population is remaining a constant size
andnot increasing.Thiscolonyisnotspace-limited–nointraspecificcompetitionforspace –however
as the colony is close to the Beaufort Island colony, the recent increase in space there (due to ice
regression) couldmeanthatif BeaufortIslandhas more suitable conditions,individualsmaymigrate
to that colony instead of remaining at Cape Bird (Lyver, 2014).
Expectations for the Future:
As MPAs are meant to help support the ecosystem and species living within the area protected, we
are hopingthatcolonypopulationsizesatall 3 sites forthisstudywill increase,astheyhave between
2016-2018, accordingto the Adélie PenguinCensus.We alsohope thatthe establishmentof the Ross
SearegionMPA isallowingthe individualhealthof the penguinstothrive.Asone of the targetsof the
Ross Sea regionMPA is to protect the ecosystemandbiodiversity(Brooks,2021), the populationsat
all coloniesshouldundergoadecreaseinintraspecificcompetitionfor predation,asfishing(especially
krill fisheries) has been stopped,or at least limited, in their hunting grounds.However, it is unknow
how the anthropogenic impacts increasing climate warming will affect the Ross Sea ecosystem as a
whole –there maybe newproblemsthatarise thatweren’taroundinthe past,oreven atpresentday
that could affect P. adeliae populations. Unfortunately, to completelyunderstand how the changing
climate will affectP.adeliaepopulations,we mustcompletelyunderstandthe dynamicsof biological
cycles within the Southern Ocean and discover how they are expected to adapt to the foreseen
changes(Xavier,2016). AsP. adeliae are indicatorspeciesof the SouthernOcean,any data collected
from thisstudycan partiallyhelpusunderstandthe healthof the SouthernOceanand how different
natural and anthropogenic impacts are affecting it.
If the populations don’t continue to increase or remain constant, then management efforts of the
MPA should be re-evaluated to see if there are any obvious reasons causing the population size
decreases. Aslongasthe managementeffortsremainenforcedthenthe MPA establishment thenwe
predict the MPA shouldn’t have a negative effect on the colonies – assuming no major
natural/anthropogenic disasters occur, like the icebergs of 2000/2001 that caused the build-up of
excessseaice. The MPA beingaGPZ aroundthe coast shouldhelplimitanthropogenicimpactsinthe
foraging ground of all 3 sites, however any possible anthropogenic impacts that could affect
population sizes or colony and individuals health should be considered when analysing the data.
Studyingthe healthof individualsandanalysingthe overall healthof the colonyshouldindicate that
both are healthy, if the MPA is being effective and supporting the Ross Sea ecosystem as was
considered to support the ecosystem during its establishment.
Applicability and Uses:
Data collectedthroughoutthisstudycanandshouldbeusedbyscientistsstudyingtheSouthernOcean
and Antarctica. The data can be applied to different mathematical and computer models to predict
future trendsof populations sizesof multiple colonies aswell as the healthof these colonies –these
modelscouldbe appliedtoother colonies,notusedinthis study, in the Ross Sea and possiblyother
parts of Antarctica. AsP.adeliae are sensitivetoclimate change (Wilson,2001), informationfromthis
studycan be used to showcorrelationsbetweenpastclimate eventsandpopulationsizes,aswell as
predicting how future climate event could affect the populations, using past events as a baseline.
Estimations on how local ecosystems may be affected in the future could also be provided from
applying data to different models.
As an indicatorspecies, dataaboutP.adeliae can usedto evaluate the healthof the local ecosystem,
so the amount of data collected on this species is invaluable. Researchers have estimated that
increasingpopulationsizescouldbe correlatedto the increasingandoverabundant presence of their
favourite andmostlyconsumed prey,krill – the increase of krill abundance inthese areas ispartially
due to decreasing sea ice (King,2018), but future data collected from other studies focusing on krill
abundances inthe Ross Seacouldalsoprove that by vastlydecreasingthe areainwhichkrill fisheries
and researchers can catch krill may also show increases in krill available for predators.
By considering if and how the Ross Sea region MPA has affected the local penguin colonies in this
study,countriesproposingnewMPAsaroundAntarcticain the future,can hopefullyuse keyfindings
found within this study to support how their MPA could affect the any local penguin colonies and
evaluate how different management efforts used in the Ross Sea region MPA have been either
effective orineffective andwhatmanagementeffortsshouldbe usedintheirMPA. A similarprocess
to this was completed in the Central Mediterranean; scientists there assessed the coastal fish
assemblages before the establishment and proposal of a MPA in that area. Using the data they
collectedthey identifiedareasof majorconcernforMPA zoningandlookedatthe role of formulating
a zoning proposal. This study ended up being very successful and informative for the set up of that
MPA within the Central Mediterranean area (La Mesa, 2017).
Budget:
Equipmentformeasuringweightandheightof individualsforeachsite (IncludesAdamEquipment
CPWplus-75Ldigital platformscalesandstandardtape measure) - $1 500 total
Dronesfor aerial view(chose SwiftTrainerAutonomousDrone),one persite - $45 000 total
3 x UAV drone technicianswith6monthspay - $25 000 each
9 x Researchscientistswith6monthspay - $35 000 each
12 x volunteersworkingwithnopay
Misc. (includingtravel andpre-deploymentmedical exams,shipmentof new partsif technology
needsfixing) - $150 000
Total directcosts - $586 500
Indirectcosts(44% of direct costs) - $258 060
Total - $844 560
The salariesare justbasedof one seasonof data collection (spending6monthsinAntarctica),with
the hope that thiscouldbe set upas a long-termmonitoringproject,the projectwouldcostan
additional $390 000 in salariesplustravel toand fromstationandbeginningandendof eachseason.
Flightsare conductedbyUnitedStatesAirForce (fromUS) and was unable tofindpricesforthese.
WhenworkinginAntarctica,there isno needtobudgetforstationuse,suitable clothing,pre-
deploymenttraining, permitsoranyotherlogistical costs asall are coveredbythe U.S. Antarctic
Program – whichisa part of the National Science Foundation.
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Research Proposal - Are the Adélie penguin, Pygoscelis adeliae, populations with breeding colonies in the Ross Sea being affected by the establishment of the Ross Sea region Marine Protected Area?

  • 1. Are the Adélie penguin, Pygoscelis adeliae, populations with breeding colonies in the Ross Sea being affected by the establishment of the Ross Sea region Marine Protected Area? Elizabeth Howarth University of North Carolina, Wilmington BIO 484: Research Methods in Biology Dr. Troy Alphin November 30, 2021
  • 2. Rational: The focusonthisstudyistoevaluate how the populationsizeandhealthof Adélie penguin,Pygoscelis adeliae, colonies at Cape Royds, Cape Bird and Cape Crozier have changed over time, especially in relation to the Ross Sea region Marine Protected Area, MPA, established in 2017 and considering major environmental and biological factors that could have an effect on these populations. We will continue tocollectnewdataannually tolookatanyaffectstheRossSearegionMPA ishavingonthese populations. Using data about population sizes of coloniesand health of individuals from within the colonies,wewillevaluatethe overallhealthofthe colonies andpredicthowwe expectthemtochange in the near future. This is an important study as P. adeliae are an indicator species for their local ecosystem – the health of the penguin colonies reflects the health of the local ecosystem. Introduction: Marine Protected Areas, MPAs: MPAs involve the spatial zoning of a marine environment for either the conservation of: individual species, habitats or whole ecosystems through the regulation human activity within that area (Hoagland et al., 2019) and are focused in areas that are most vulnerable to natural and artificial disturbances (Australian Association for Maritime Affairs, 2012). Classifications of MPAs involve definingthe protectedareaasasimple andaccurate reflection of the proposedgoalsandapproaches (designed specifically for that individual area) as well as allowing assessmentsof associatedimpacts the MPA couldpresent,whilsthavingminimalimplications(NOAA,n.d.).The effectivenessof anMPA is presented by the unique balance of intensity of exploitation, type of management programmes implemented, and overall protection implemented in the area (WCPA, 2018). Previous studies have shownthatthe most effective MPAs all have 5keyfeatures:MPA setasa no-take zone, implemented lawsare well enforced,the MPA is establishedfor more than 10 years, it is an area greater than 100 km2 , and the zone is isolated by either deep water or sediment (Edgar, 2014).
  • 3. Antarctica and it’s corresponding waters contain many endemic and well adapted species, so it’s important that as environmental conditions begin to change (due to natural and anthropogenic- induced disturbances) we must begin to design and enforce protection projects within the most vulnerable areas to limitany disturbances to the local terrestrial and marine ecosystems(Kavanagh, 2020). It has also been suggestedthat is all MPAs, proposed and currentlyenforced, in and around Antarctica were accepted as a permanentfeature then a positive impactonmany specieswouldbe observed; some species could also show significant increase in population size (University of East Anglia, 2021). Figure 1 – proposed and existing MPAs in the Southern Ocean, surrounding Antarctica – The map shoes how the Southern Ocean is separated into 9 different domains and also shows existing continental MPAs, MPAs protecting subantarctic islands and Proposed MPAs which will protect more of the coast of the Antarctic continent (PEW Charitable Trust, 2019) The Ross Sea region MPA, which became established in December 2017 by Commission for the Conservation of Antarctic Marine Living Resources (CCAMLR) – for at least 35 years – (Dodds, 2018) includes the Ross Sea Continental Shelf, which is one of the most productive areas of the Southern
  • 4. Ocean.AsSeeninfigure 1,the RossSearegionMPA isfoundwithindomain8andcoversanextensive area; in fact, it is the world’s largest MPA at 2.09 million km2 . Figure 2 – map of Ross Sea region MPA – this map clearly shows the distribution of the different types of zones within this MPA region. (Crown, 2016) ThisMPA has3 differentlevelstypesof zoneswithinit,whichinclude:General ProtectionZones(GPZ), Special ResearchZones(SRZ) and Krill ResearchZones(KRZ) (Crown, 2016). The distributionof these 3 zones are shown in figure 2. GPZ covers the most heavily protected areas where no fishing is permitted, SRZ allow limited fishing of krill and toothfish for research only and KRZ is slightly more relaxed by allowing controlled krill fishing but still only for research (Marine Conservation Institute, 2021). Adélie Penguins, Pygoscelis adeliae: P. adeliae breed on and around the continent and consume mostly krill and other oceanic prey for food – because of this they are a good indicator species for the marine ecosystem.Previous studies that tracked P. adeliae showed they can travel thousands of kilometres during winter to feed and returnto the same colonies atthe start of theirbreedingseason(Conveyetal.,2013). Theirbreeding
  • 5. seasonbeginsinOctoberandaverage colonypeakegglayingismid-November,whichgivesthe chicks time to grow before they have to fledge their colonies by March (Barreau, 2019). Parent penguins have to use a lot of metabolic energy to raise their chicks – both parents have to spendmanyweeksfastingtolookafterthe eggornewlyhatched chick.Theytake turnstogoforaging forfood,where theyhave tocollectenoughfoodforthemandtheirchick (aschickiscurrentlyunable to swimor hunt for own food). Predation andphysiological limitsare majorbioticfactors that affect the magnitude of parental care giventothe chicks(Chappell,1993).Abioticfactorssuchastime limits and sea ice concentration may also affect foraging and breeding successes; negative correlation between increased sea ice and breeding/foraging successes have been identified. Increased ice has been associated with colder temperatures, meaning individuals must use more metabolic energy keepingwarmthanif it was a warmer year.Also increased seaice meansparentsmusttravel further to openwaterthaninotheryears –thisnotonlyincreasesforagingtrips,butalso meansparentsmust catch more food, as they require more energy to make that journey, but must still have enough to feed their chicks (Barreau, 2019). Phenological timing of the beginning of the breeding season is driven by a combination of physiological, ecological and behavioural processes as well as environmental cues prior to the breeding season. A previous study conducted at Bechervaise Island, East Antarctica showed that P. adeliae respond to changes in environmental conditions by adjusting their timings of breeding – demographic consequences less well understood. The changing environmental conditions directly impactthe penguinsbyimpactingforagingandcolonyaccessibility.Ithasbeensuggestedthat further, more pronounces environmental and phenological changes could have problematic effects on breeding populations (Emmerson, 2011). Collection of organic matter from P. adeliae at multiple abandoned colonies have beendated, using radiocarbondating, andshowthatthe therehasbeenalonghistoryof colonisationandabandonment throughout the Ross Sea region. The oldest samples so far have dated back to 45 000 years ago.
  • 6. Radiocarbon dates of multiple samples of bone, tissue and eggshell of P. adeliae confirm that the oldestcolonieswere presentfrom45 000 – 27 000 yearsbefore present(yrB.P.).There wasthen an abandonmentperioduntil8000 yr B.P. – due tothe lastadvancementof the RossIce Sheet.Between thenand presentday,there have been 2 further periods of abandonment (5 000 – 4 000 and 2 000 – 1 100 yr B.P.) that correlate to cooling periods which had unfavourable marine conditions. Finally, datingsuggestsmost moderncolonieshave all beenestablishedwithinthe past2 000 years(Emslie, 2007) Working in Antarctica: Antarcticaisa verychallengingenvironmenttoworkinandrequires alotof preparationandplanning fromeveryone onthe team –some of the majorchallenges scientistsface whenworkinginAntarctica include: challenging weather, accessibility (to research stations and to field sites), technology and equipment failure, safety and composition of the team (Sanson, 2013). Before stepping foot in Antarctica, preparation of individual members of the team and preparation for the actual science proposed tohappenmustoccur. Everymemberof the team mustundergopre- deploymenttrainingand medical testing,aswell asreceivingtheirkit,includingappropriate clothing for the environment– this ensures the safety of the team throughout their time in Antarctica and allows each team member to become familiar with how life in Antarctica is different to outside Antarctica, as well as how the research station and field sites work (National Science Foundation, 2018). AsRoss Islandis an Antarctic SpeciallyProtectedArea(ASPA) –designatedbythe Protocol on Environmental Protection to the Antarctic Treaty - a permit is required to enter and work in those areas.The permitsare allocatedby the National Science Foundation(NSF).The NSF isalsothe largest granting body within the USA, a grant is also required to work within Antarctica. (Rejcek, 2008) Wheninthe field,weathercanbe unpredictableanddangerous,ascanchange frommildto severe in the space of minutes. The use of training, completion of risk assessments and availabilityof survival bags when off base, all of these increase chance of survival if natural disasters, cold climates or
  • 7. extreme weatherwastooccurwheninthe field.Whilstinthe fieldalso,allequipment,transportation, food, and other things usually needed for the logistics of the field research are provided by the granting body, the trade-off being there is some part of your schedule that you can’t control; for example youcanonlygotodo yourfieldworkaslongasthere isroomat the local researchstation for when you are not in the field. (Vervoort, 2011) Objectives:  Compare P. adeliae populationgrowthsof colonies from1983 – presentandinto the future. To do this I will: o Use past collected data of aerial counts of population size for each colony at each study site o Conductnew aerial andground populationsize countsforeach colonyat each study site o Collectdatatocalculate how manychicksare beingraisedpercolonyperyear ateach study site  Evaluate health of the penguin colonies. To do this I will: o Measure height, weight and sex of individual adults as soon as the exit the water at the beginning of the breeding season at each study site o Measure weightof chicksjustbefore theyenterthe water,astheyfledge the colony, at the end of the breeding season at each study site  Evaluate how colony population sizes have changed over time: o See if the MPA establishment has had any effect of the colonies o Evaluate how the health of the colonies and individuals within the colonies are changing o compare datafromdifferentyearsandalsoevaluate ifonecolonyismore healthy/has more healthy individuals than another colony
  • 8. o Predict how the population sizes may change in the near future o This evaluation will include constructing graphs and completing statistical tests Methods: Study Sites: Figure 3 - This map of Ross Island, this island can be shown in respect to the Antarctic continent in the small diagram of Antarctica in the left, bottom corner. On the Island, the 3 labels show the location of the 3 different colonies I’m going to look at throughout my experiment. These colonies are at Cape Royds (indicated by yellow dot), Cape Bird (indicated by purple dot) and Cape Crozier (indicated by pink dot). (Mike, 2013) Figure 3, showingRossIsland and the 3 P. adeliae colonysitesI’ve chosen to use for my study.Cape Royds represents smaller colonies, Cape Bird represents medium sized colonies and Cape Crozier represents larger colonies.As well as representing a wide size range of colonies, all 3 sites have had data collected consecutivelyoverthe pastfew decades,meaningall 3sitesare representable for the studyand allowmaximumreliabilityof the analysiswe will be completingwithinthisstudy. Ontopof
  • 9. this,eachlocationhasitsown slightlydifferentweatherconditionsandchallenges,makingthe results further representative of the whole Ross Sea region. Data Collection: The aerial countsof populationsizescollectedinpreviousyearsare sourcedfromthe Adélie Penguin Census,whichisprovidedbyAntarcticaNew Zealand –agovernmental agencythatisresponsiblefor science and environmental protection activities that New Zealand complete within Antarctica (Antarctica New Zealand, 2021) All data collected as a part of this study will be within the guidelines provided in the CCAMLR Ecosystem Monitoring Programme (CEMP) Standard Methods handbook. These standard methods were establishedtoregulate the methodof datacollection;asall data collectedmustbe sharedwith CCAMLR, it allows the formation of standardised data series which are freely accessible (CCAMLR, 2014) Firstly,inregardtocollectingdatatohelpme analysethe healthof the colonybylookingatindividuals withinthe colonies,Iwill collectdataof adultsastheyarrive at the breedingsitethe beginningof the breedingseasonanddataonchicksastheyfledgethe breedingsiteatthe endof the breedingseason. Whencollectingthe weight,sex andheightof adult penguins,astheyarrive ontobeachof theircolony, I will followStandardMethodA1(v3). Whencollectingthe weightof chicksasthey fledgetheircolony via the beach, I will follow Standard Method A7 (v4) procedure A. Secondly,inregardtocollectingdatatocontinuemonitoringthe populationsizes ateachcolony,Iwill complete aerial counts, using UnmannedAerial Vehicle (UAV) drones, and ground counts,as well as calculatingthe numberof chicksraisedpercolony.Toconductgroundpopulationcounts,Iwill follow StandardMethodA3A (v4). Whilstconductingaerial populationcounts,Iwill followStandardMethod A3B (v1). Whist collecting data about breeding success (which will be used when calculating chicks raised per colony), I will follow Standard Method A6 (v5) Procedure C.
  • 10. All methods are explained in detail in CCAMLR Ecosystem Monitoring Program Standard Methods handbook, revised in June 2014. Data Representation and Analysis: Populationsizesatall 3sitesare andwill be representedinasimplelinegraph. Plottingall mydataon only1 setof axisallowsforeasieridentificationof anypatternsoccurringatthe same timeatdifferent colony sites.Italsoallows foran overall trendstobe observed. We decidedtoadda secondaryx-axis forCape Royds,so the trendof all 3 sitescanbe easilyobserved,onlyhavingasingle x-axismeantthe trends of Cape Royds couldn’t be observed well. Statistical T-tests, using mean population sizes for pre- and post- MPA establishment could also be helpful – this will me more accurate as collect more data as currently only have 2 data points, per colonysite.T-testscouldalsocompare groundpopulationsizecountsandaerial populationsize counts from the same year to identify if there is any significant differences between the 2 methods of collecting the same data. A previous study with a simulated colony set-up suggests that population sizes collected from Unmanned Aerial Vehicles (UAV), compared to ground-based counts,are more accurate (Hodgson, 2018). To evaluate breeding success, we will compare the number of eggs laid to the number of chicks fledging.Thiswill allowustocalculate the successrate of parentingperyearat eachcolony,withthis data we can compare parental successrates betweencoloniesand view the trendof how successful breeding at a single colony is from year to year. The constructionof a populationmodel,fromthe datawe will collectcanallow usandotherscientist to studythe populationdynamicsof eachcolonysite.The modelcouldthenbe appliedwithdifferent parameters to estimate how the population is expected to change in the near future with those set parameters.
  • 11. Results: Analysisof Past Data: As previously stated, this data is from the Adélie Penguin Census and shows aerial population size counts from the early 1980s to present day – unfortunatelydue to COVID-19, no data was collected inyears2019 and2020, meaningthere willbe atleasta2-yeargapinmyaerial populationsizedataset. Hopefullyas we get more data over the next few years, we can make accurate estimations on what the data probably would have shown if data was collected in those years. Figure 4 - – aerial survey data from 1983 – 2018 based on data from Adélie Penguin Census, Antarctica New Zealand, for Cape Royds, Cape Bird and Cape Crozier. In the Census, Cape Bird was split into North, Middle and South and Cape Crozier was split into West and East – in this graph I have combined them to get total counts for each colony area. There was no count collected: Cape Bird North 2000, Cape Bird Middle 2008 and Cape Crozier West 2000. No data collected for these times can explain the abnormalities for these years within my graph (Cape Bird 2000 and 2008 and Cape Crozier 2000). Previouslycollected data,representedinfigure 4, showsmildannual variety duetovariationincensus dates, weather and climatic differences throughout the years and differing sea ice content 0 500 1000 1500 2000 2500 3000 3500 4000 4500 0 50000 100000 150000 200000 250000 300000 350000 19831985 1987 1989 1991 1993 1995 1997 1999 200120032005 2007 2009 2011 2013 2015 2017 number of penguins at Cape Royds number of penguinsins at Cape Bird and Cape Crozier Year Cape Bird Cape Crozier Cape Royds
  • 12. surroundingthe breedingsites(Taylor,1990).Previouscomparisonsof the Adélie PenguinCensuswith local climatic events occurring at the same time have shown that generally,years with increased temperaturesinthe Ross Sea regionhave positivelyinfluenced P.adeliae populationsinthose years – thismay be due toeasieraccesstoopenwater, increasedlocalproductivityof the RossSea(causing increased food availability), lower winter mortality,enhanced breeding success or a combination of these factors (Taylor, 1990). All colonies, especially Cape Royds and Cape Crozier were drastically affectedbythe icebergs in2000/2001 that changedthe local environmentaroundthe colonysites, in those years.These icebergshadanegative impactonthe coloniesbreedingatthose sites andcaused decreased successful reproduction and decreased survival rates in the years the icebergs were present. Cape Royds: In 2000, multiple large icebergs broke off the Ross Ice Shelf and caused lots of sea ice to build up, become stuckand unable to melt.Thiswas a disadvantage tothe Cape Roydscolonyand because of thisin2000 lesschickswere produced –probablymostlyduetothe increasedenergyneededtoaccess openwaterduring the breedingseasontoforage for foodfor themselvesandtheirchicks.Aswell as this, many breeding pairs moved from Cape Royds to other local breeding sites, including Cape Bird and Beaufort Island. Luckily, over the next few years as the sea ice broke up, the colony recovered, and the population size of the colony increased again (Rejcek, 2008). Since 2000, the population at Cape Royds has remained to increase and in the next few years could be expectedtobe backatthe same approximate size asitwasbeforethe devastatingincidentin2000. Thisproveshowdelicate these populationsare tochangesintheirenvironment andfurthersupports whyitissoimportanttoprotecttheirlocal environments;ithastakenthiscolony>15yearstorecover, and is still recovering, however many colonies that face disaster end up becoming completely abandoned and separated to multiple other local colonies.
  • 13. Cape Crozier: Cape Crozier, the largest colony in my study, has previously been thought to be a self-regulating population andbecause of this,unlikelytocollapse because of populationpressure –ithas alsobeen suggestedthatmore extreme weatherandanthropogenicimpactsare likelytoaffectthispopulation inthe future (Rejcek,2008). Asa largercolony,individualsthatbreedatthissite are requiredtospend more energy to collect food during foraging trips, this is due to increased intraspecific competition between individualswithin this population. Duration of the foraging trips and metabolic rates are likely to be increased compared to the other 2 colonies within this study (Balance, 2009). During1980’s and 1990’s there wasa slightdeclineinpopulationsize.Due tosome missingdatafrom Cape Crozier in the year 2000, it is unknown exactly when the sudden decrease in population size occurred. However the arrival of giant icebergs, B15A and C16, in the Ross Sea in January 2001 (Kooyman,2007), can explainthe decrease of >89 000 individuals between the years 1999 and 2001. Since then, the population has drastically increased,on average, with 2018’s data showing a colony size of over 300 000 individuals – up from approximately 67 000 individuals in 2001. Cape Bird: Cape Bird,the most northernsite withinthisstudy,sits at the tip of Ross Island.The populationsize of the colony at this site has remained fairlyconstant from 1983-2018 (the years we have data for), showing no major variations in population size. This is probably due to the fact this site hasn’t been affected by any major weather disturbances or anthropogenic disturbances that would affect reproductionrates or survival rates.It has beensuggestedthatfood may be limited,partiallydue to environmental stochasticity, and this could explain why the population is remaining a constant size andnot increasing.Thiscolonyisnotspace-limited–nointraspecificcompetitionforspace –however as the colony is close to the Beaufort Island colony, the recent increase in space there (due to ice regression) couldmeanthatif BeaufortIslandhas more suitable conditions,individualsmaymigrate to that colony instead of remaining at Cape Bird (Lyver, 2014).
  • 14. Expectations for the Future: As MPAs are meant to help support the ecosystem and species living within the area protected, we are hopingthatcolonypopulationsizesatall 3 sites forthisstudywill increase,astheyhave between 2016-2018, accordingto the Adélie PenguinCensus.We alsohope thatthe establishmentof the Ross SearegionMPA isallowingthe individualhealthof the penguinstothrive.Asone of the targetsof the Ross Sea regionMPA is to protect the ecosystemandbiodiversity(Brooks,2021), the populationsat all coloniesshouldundergoadecreaseinintraspecificcompetitionfor predation,asfishing(especially krill fisheries) has been stopped,or at least limited, in their hunting grounds.However, it is unknow how the anthropogenic impacts increasing climate warming will affect the Ross Sea ecosystem as a whole –there maybe newproblemsthatarise thatweren’taroundinthe past,oreven atpresentday that could affect P. adeliae populations. Unfortunately, to completelyunderstand how the changing climate will affectP.adeliaepopulations,we mustcompletelyunderstandthe dynamicsof biological cycles within the Southern Ocean and discover how they are expected to adapt to the foreseen changes(Xavier,2016). AsP. adeliae are indicatorspeciesof the SouthernOcean,any data collected from thisstudycan partiallyhelpusunderstandthe healthof the SouthernOceanand how different natural and anthropogenic impacts are affecting it. If the populations don’t continue to increase or remain constant, then management efforts of the MPA should be re-evaluated to see if there are any obvious reasons causing the population size decreases. Aslongasthe managementeffortsremainenforcedthenthe MPA establishment thenwe predict the MPA shouldn’t have a negative effect on the colonies – assuming no major natural/anthropogenic disasters occur, like the icebergs of 2000/2001 that caused the build-up of excessseaice. The MPA beingaGPZ aroundthe coast shouldhelplimitanthropogenicimpactsinthe foraging ground of all 3 sites, however any possible anthropogenic impacts that could affect population sizes or colony and individuals health should be considered when analysing the data.
  • 15. Studyingthe healthof individualsandanalysingthe overall healthof the colonyshouldindicate that both are healthy, if the MPA is being effective and supporting the Ross Sea ecosystem as was considered to support the ecosystem during its establishment. Applicability and Uses: Data collectedthroughoutthisstudycanandshouldbeusedbyscientistsstudyingtheSouthernOcean and Antarctica. The data can be applied to different mathematical and computer models to predict future trendsof populations sizesof multiple colonies aswell as the healthof these colonies –these modelscouldbe appliedtoother colonies,notusedinthis study, in the Ross Sea and possiblyother parts of Antarctica. AsP.adeliae are sensitivetoclimate change (Wilson,2001), informationfromthis studycan be used to showcorrelationsbetweenpastclimate eventsandpopulationsizes,aswell as predicting how future climate event could affect the populations, using past events as a baseline. Estimations on how local ecosystems may be affected in the future could also be provided from applying data to different models. As an indicatorspecies, dataaboutP.adeliae can usedto evaluate the healthof the local ecosystem, so the amount of data collected on this species is invaluable. Researchers have estimated that increasingpopulationsizescouldbe correlatedto the increasingandoverabundant presence of their favourite andmostlyconsumed prey,krill – the increase of krill abundance inthese areas ispartially due to decreasing sea ice (King,2018), but future data collected from other studies focusing on krill abundances inthe Ross Seacouldalsoprove that by vastlydecreasingthe areainwhichkrill fisheries and researchers can catch krill may also show increases in krill available for predators. By considering if and how the Ross Sea region MPA has affected the local penguin colonies in this study,countriesproposingnewMPAsaroundAntarcticain the future,can hopefullyuse keyfindings found within this study to support how their MPA could affect the any local penguin colonies and evaluate how different management efforts used in the Ross Sea region MPA have been either effective orineffective andwhatmanagementeffortsshouldbe usedintheirMPA. A similarprocess
  • 16. to this was completed in the Central Mediterranean; scientists there assessed the coastal fish assemblages before the establishment and proposal of a MPA in that area. Using the data they collectedthey identifiedareasof majorconcernforMPA zoningandlookedatthe role of formulating a zoning proposal. This study ended up being very successful and informative for the set up of that MPA within the Central Mediterranean area (La Mesa, 2017). Budget: Equipmentformeasuringweightandheightof individualsforeachsite (IncludesAdamEquipment CPWplus-75Ldigital platformscalesandstandardtape measure) - $1 500 total Dronesfor aerial view(chose SwiftTrainerAutonomousDrone),one persite - $45 000 total 3 x UAV drone technicianswith6monthspay - $25 000 each 9 x Researchscientistswith6monthspay - $35 000 each 12 x volunteersworkingwithnopay Misc. (includingtravel andpre-deploymentmedical exams,shipmentof new partsif technology needsfixing) - $150 000 Total directcosts - $586 500 Indirectcosts(44% of direct costs) - $258 060 Total - $844 560 The salariesare justbasedof one seasonof data collection (spending6monthsinAntarctica),with the hope that thiscouldbe set upas a long-termmonitoringproject,the projectwouldcostan additional $390 000 in salariesplustravel toand fromstationandbeginningandendof eachseason. Flightsare conductedbyUnitedStatesAirForce (fromUS) and was unable tofindpricesforthese. WhenworkinginAntarctica,there isno needtobudgetforstationuse,suitable clothing,pre-
  • 17. deploymenttraining, permitsoranyotherlogistical costs asall are coveredbythe U.S. Antarctic Program – whichisa part of the National Science Foundation.
  • 18. References: AntarcticaNewZealand (2021), Home, URL: https://www.antarcticanz.govt.nz/ AustralianAssociationforMaritime Affairs (2012) Marine ProtectedAreasProposedforEast Antarctica, Australian Maritime Digest 217 p. 1-2 Ballance L.T., AinleyD.G.,BallardG.,BartonK. (2009) Anenergeticcorrelate betweencolony size and forging effort in seabirds, an example of the Adélie penguin Pygoscelis adeliae, Journal of Avian Biology 40, p. 279-288, DOI: https://doi.org/10.1111/j.1600-048X.2008.04538.x Barreau E., Ropert-Coudert T., Delord K., Barbraud C., Kato-Ropert A. (2019) Scale matters: sea ice and breeding success of Adélie penguins, Polar Biology 42, p. 1405-1410, DOI: https://doi.org/10.1007/s00300-019-02531-2 Brooks C. M., Bloom E., Kavanagh A., Nocito E. S., Watters G. M., et al. (2021) The Ross Sea, Antarctica: a highly protected MPA in international waters, Marine Policy 134, DOI: https://doi.org/10.1016/j.marpol.2021.104795 CCAMLR (2014 (revised)) CCAMLR Ecosystem Monitoring Programme Standard Methods, Tasmania: CCAMLR Chappell M.A.,JanesD. N.,ShoemakerV.H.,Bucher T. L., MaloneyS. K.(1993) Reproductive efforts in Adélie penguins, Ecology 74(4), p. 1204-1215 URL: https://www.jstor.org/stable/1940491 Convey P., Brandt A., Nicol S. (2013), Life in a cold environment, Antarctica: Global Science from a Frozen Continent (Walton D. W. H.), Cambridge University Press, p. 167-168 Crown (2016) Ross Sea region Marine Protected Area New Zealand Foreign Affairs & Trade URL: Ross Sea region Marine Protected Area | New Zealand Ministry of Foreign Affairs and Trade (mfat.govt.nz)
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