Chronic captivity stress in wild animals is highly species-specific

© The Author(s) 2018. Published by Oxford University Press.This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.

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Volume 7 • 2018 10.1093/conphys/coz093

Review article

Chronic captivity stress in wild animals is highlyspecies-specificClare Parker Fischer and L. Michael Romero*

Department of Biology, 200 College Ave. Tufts University, Medford, MA 02155 USA

*Corresponding author: Department of Biology, Medford, MA 02155, USA. Email: [email protected]

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Wild animals are brought into captivity for many reasons—conservation, research, agriculture and the exotic pet trade. Whilethe physical needs of animals are met in captivity, the conditions of confinement and exposure to humans can result inphysiological stress. The stress response consists of the suite of hormonal and physiological reactions to help an animal survivepotentially harmful stimuli. The adrenomedullary response results in increased heart rate and muscle tone (among othereffects); elevated glucocorticoid (GC) hormones help to direct resources towards immediate survival. While these responsesare adaptive, overexposure to stress can cause physiological problems, such as weight loss, changes to the immune system anddecreased reproductive capacity. Many people who work with wild animals in captivity assume that they will eventually adjustto their new circumstances. However, captivity may have long-term or permanent impacts on physiology if the stress responseis chronically activated. We reviewed the literature on the effects of introduction to captivity in wild-caught individuals onthe physiological systems impacted by stress, particularly weight changes, GC regulation, adrenomedullary regulation andthe immune and reproductive systems. This paper did not review studies on captive-born animals. Adjustment to captivityhas been reported for some physiological systems in some species. However, for many species, permanent alterations tophysiology may occur with captivity. For example, captive animals may have elevated GCs and/or reduced reproductivecapacity compared to free-living animals even after months in captivity. Full adjustment to captivity may occur only in somespecies, and may be dependent on time of year or other variables. We discuss some of the methods that can be used to reducechronic captivity stress.

Key words: stress, captivity, glucocorticoids, reproduction, immune

Editor: Steven Cooke

Received 25 July 2019; Revised 4 October 2019; Editorial Decision 13 October 2019; Accepted 13 October 2019

Cite as: Fischer CP and Romero LM (2018) Chronic captivity stress in wild animals is highly species-specific . Conserv Physiol 7(1): coz093;doi:10.1093/conphys/coz093.

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IntroductionThe tens of thousands of vertebrate species on this planet areadapted to every condition from the Arctic to the tropics andfrom the mountain tops to the ocean depths. For all species,the environment contains both predictable changes (e.g. day–night transitions or seasonal variation) and unpredictable,

uncontrollable threats to homeostasis and survival (Romeroand Wingfield, 2016). Vertebrates have evolved a suite ofdefenses against the myriad unpredictable ‘shocks that fleshis heir to’ (Shakespeare, Hamlet, 3.1)—a set of conservedphysiological responses known as the ‘stress response’. Whilethe stress response can help an animal survive a threateningevent, if noxious conditions are repeating or unrelenting two

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..........................................................................................................................................................Review article Conservation Physiology • Volume 7 2018

physiological changes take place. First, the reactive scope ofthe animal shrinks thereby decreasing the animal’s abilityto cope (Romero et al., 2009). Second, the stress responseitself can begin to cause physiological problems, a conditionknown as ‘chronic stress’. Even though there is no generallyagreed upon definition of chronic stress or the time-frame ofits onset, long-term stressor exposure or chronic stress, canlead to weight loss, immunosuppression, reproductive failureand psychological distress (Sapolsky et al., 2000). Becausethe stress response occurs when situations are perceived asthreatening, regardless of whether the animal is experienc-ing physical damage, a drastic change of conditions canlead to symptoms of chronic stress even when the animalis unharmed. Consequently, when a wild animal is broughtinto captivity for the first time, symptoms of chronic stresscan occur even though the physical needs of the animal areattended to.

In captivity, animals are provided with shelter and amplefood. Nevertheless, captivity can often result in negative phys-iological outcomes, particularly for newly-captured animals.The conditions of captivity can be perceived as threatening,and if the perceived threat does not decrease, symptoms asso-ciated with chronic stress may result. The sources of stress incaptivity are many, including cage restraint, human presence,an unfamiliar environment, and other, more subtle stressors,such as artificial light conditions (reviewed in Morgan andTromborg, 2007). When wild animals are newly broughtinto captivity, it is frequently for research, conservation, agri-culture (e.g. fisheries) or the exotic animal trade. To keepthese animals healthy, symptoms of chronic stress should beminimized or eliminated. It is often assumed that with time,animals will adjust to captivity conditions and stress willdisappear. Indeed, many animals seem to thrive in captivity.Unfortunately, many other species do not (Mason, 2010). Inthis review, we surveyed the literature to answer the followingtwo questions: do wild animals eventually adjust to captivityconditions? And if so, how long does the period of adjustmenttypically take? This literature survey exclusively addressedwild animals introduced to captivity and not animals bornin captivity.

We focused on several aspects of physiology that maybe particularly affected by long-term stressor exposure.The acute stress response involves many behavioral andphysiological changes, including activation of two hor-monal pathways. The adrenomedullary response occurswithin seconds of the onset of a stressor (Romero andWingfield, 2016). The catecholamine hormones epinephrineand norepinephrine are rapidly released from the adrenalmedulla. These cause an increase in heart rate, as well asan increase in muscle tone, an increase in blood pressureand other physiological and behavioral changes that enablean animal to survive a sudden stressor, such as a predatorattack. The second hormonal response is initiated withinminutes of the onset of a stressor, when a hormonalcascade triggers the synthesis and release of glucocorti-coids (GCs)—steroid hormones that have wide-ranging

effects on the body (Romero and Wingfield, 2016). Whilebaseline levels of GCs help regulate metabolism, increasedlevels trigger an ‘emergency life history stage’, (Wing-field et al., 1998), where resources and behaviors aredirected towards survival of the crisis and away fromlong term investments. GCs have a strong impact onthe immune and reproductive systems (Sapolsky et al.,2000). In this review, we focus on captivity’s effects onmass (one of the best-documented outcomes of chronicstress), GC concentrations and the immune, reproductiveand adrenomedullary systems. We also document howthe adjustment to captivity is impacted by time of yearand how captivity effects persist after release. Finally, wediscuss some of the ways that captivity stress may bemitigated.

MethodsWe surveyed the literature and gathered studies that com-pared wild-caught animals as they adjusted to captivity. Weconducted a literature search through Web of Science usingthe search terms ‘captivity’ and ‘stress’ and ‘physiology’ or‘endocrinology’ and related words. Because many papersreported on aspects of the stress response on animals thatwere in captivity but did not examine the effects of captivityitself, we were unable to devise search terms that includedthe studies we were interested in but excluded other researchon stress in wild animals. We therefore devised the followingcriteria to determine whether papers should be included:(i) wild species were brought into captivity and physiologicalvariables measured over the days to months of adjustmentto captive conditions OR (ii) wild-caught captive animalswere compared to free-living conspecifics AND (iii) the totalcaptivity duration was at least 3 days (we did not includethe many studies that measure only the acute stress effects ofcapture in the first 30 min to 48 hours). We further excludedtwo broad types of studies. One, we excluded studies wherewe could determine that all captive animals were captive-bred,as we were specifically interested in how well wild animalscan adjust to captive conditions when taken from the wild(though we included some studies where the origin of captiveanimals was unclear). Second, we excluded studies of wildanimals undergoing rehabilitation because it is not possibleto distinguish between responses to captivity and responses toclinical interventions in animals that were injured or sick atcapture. Once we had created a list of papers, we also checkedthe cited references of these studies for any important worksour search terms missed.

There are many studies that focused on behavioral changesin captivity. However, the variables measured can be quitespecies-specific and difficult to interpret in a context of stress.Although we recognize the importance of behavior for thewelfare of wild animals (reviewed in McPhee and Carlstead,2010), we limited our focus to studies that included somephysiological measurements (e.g. weight changes, hormoneconcentrations or immune measurements).

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We found little standardization in experimental design inthe papers examining the effect of captivity on physiology.We visually summarize the four most common experimentaldesigns in Fig. 1. Many researchers compared animals thathad been exposed to captivity (duration: 3 days to severalyears) to those that had not (Fig. 1A). In some cases, the free-living population was sampled when the captive populationwas initially captured. This was often the case in specieswhere only a single blood sample could be drawn from anindividual. In other studies, the free-living population wassampled entirely separately from the captive group. This wasoften the case for long-term captives, such as zoo-housedanimals. Another common technique was to take a singlepre-captivity sample and a single post-captivity sample onthe same animal (duration of captivity 5 days to 3 months)(Fig. 1B). Other researchers used repeated sampling tech-niques—either sampling the same individual multiple times,or keeping different individuals in captivity for different dura-tions before sampling. Some focused narrowly on the first fewdays of captivity (Fig. 1C), while others did not take a secondsample until several weeks had passed (Fig. 1D). Furthermore,captive conditions varied between studies, with some studiesbringing animals into closed indoor situations, whereas othersplaced captive animals into open outdoor pens. We consideredeach situation to represent captivity, but we were not able tocontrast any differences in responses.

We created summary figures for the trends we observed inweight, GC hormones and the immune system with respect tocaptivity duration (Figures 2–4). To construct these, we talliedthe total number of studies that reported on the variablefor a particular time window and determined whether thevariable was above, below or equal to what it was in a free-living population. If a single report showed two differentpatterns (e.g. males and females had different patterns or twospecies were reported in the same paper), each pattern of wasincluded separately. Therefore, one ‘study’ might be includedmultiple times in the figure. This also holds true for reportingpatterns in the literature in the text and in the tables—ifone paper reported multiple patterns in different groups ofindividuals, it was included more than once in calculatingpercentages of studies and was given more than one line on thetables. We did not include studies in the figures if there weremarked seasonal differences in one species (see Section 9 forseasonal differences).

Because most of the papers we collected did not reporteffect sizes, a formal meta-analysis was not possible. Conse-quently, we focused on qualitative differences.

Mass and body condition in captivityAfter being brought into captivity from the wild, animals fre-quently experience a period of weight loss (Table 1). In 64%of studies (23 of 36), there was a documented decrease in massassociated with captivity during at least the initial captureperiod. Weight loss in captivity is likely to be attributable to

Figure 1: Examples of experimental designs to assess the effects ofcaptivity on a physiological variable (e.g. GC concentration) (A)Comparison of captive individuals to free-living populations. In somecases, the free-living samples were acquired at the same time thatthe study population was brought into captivity. In other designs, thefree-living samples were taken from entirely different populationsthan the origin of the captive animals (e.g. comparing zoo-housedanimals to wild conspecifics). (B) Each individual measuredimmediately at capture and again after a period of captivity (days tomonths). (C and D) Each individual measured immediately at captureand resampled at multiple timepoints. Some studies focused on thefirst few days, with sampling points relatively close together (C).Other studies may not have taken another sample until several weeksafter capture (D).

chronic stress. Captive animals are not calorically restricted(as long as they choose to eat), which is not always thecase in the wild, and they are not likely to use as manycalories because cage restraint limits the amount of exercisethat an animal can get in a day. Experimentally inducedchronic stress has been demonstrated to lead to weight lossin mammals (e.g. Flugge, 1996), birds (e.g. Rich and Romero,2005) and fish (e.g. Peters et al., 1980). In fact, weight lossis the most consistently seen effect of chronic stress (Dickensand Romero, 2013).

In 39% of studies where animals lost weight (9 of 23),the animals eventually regained the weight they had lost. Insome cases, weight loss may be very transitory and last onlya couple of days. For example, North Island saddlebacks (abird native to New Zealand) lost weight on the first day ofcaptivity, but by Day 3, they had not only regained weight,

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Figure 2: Weight change as a function of captivity duration. Data were collected from 35 studies listed in Table 1, with studies counted multipletimes if they measured multiple time points after introduction to captivity. The number of species that lost weight in captivity (relative to wild,free-living animals) decreased with captivity duration.

Figure 3: Change in baseline or integrated GCs as a function of captivity duration. Data were collected from the 47 studies listed in Table 3 thathad a well-defined wild baseline value (i.e. plasma samples were collected within minutes of capture; fecal or urine samples were collectedshortly after capture), with studies counted multiple times if they measured multiple time points after introduction to captivity. This figure doesnot include studies with seasonal effects on the GC response to capture.

they were heavier than they were at capture (Adams et al.,2011). Transitory weight loss may be related to adjustment tothe captive diet and not to major physiological problems. Inother species, it may take weeks or months to regain the lostmass. House sparrows lose weight by Day 5–7 of captivity(Lattin et al., 2012; Fischer and Romero, 2016). In a long-term study of the species, they did not regain the weight they

had lost for nearly 5 weeks (Fischer et al., 2018). Similarly,female possums lost weight for 5 weeks before beginning togain again, and although they were kept for 20 weeks, theynever fully recovered their lost weight (Baker et al., 1998). In61% of studies (14 of 23), weight that was lost was neverregained, though the studies may not have been long enoughfor weight to stabilize.

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Figure 4: Changes in neutrophil or heterophil (N or H:L) to lymphocyte ratio in captivity as a function of time. Data were collected from 19studies listed in Table 4, with studies counted multiple times if they measured multiple time points after introduction to captivity. The percent ofstudies that recorded elevated N or H:L ratio in captivity decreased with the amount of time spent in captivity.

In some cases, weight loss depended on the characteris-tics of the animal at capture. For example, female possumslost weight over the first 5 weeks of captivity but somemales gained weight during that period (Baker et al., 1998).When curve-billed thrashers were captured, birds from urbanenvironments had higher body condition than desert birds,but after 80 days in captivity, their body conditions hadconverged to an intermediate value (Fokidis et al., 2011).Captivity may impact individuals differently depending onsex, population of origin or other individual characteris-tics, including transitory physiological states. (See Section 9for the effects of time of year on the ability to adjust tocaptivity.)

Weight loss was not the only pattern seen in captivity.In 17% of studies (6 of 36), animals gained mass abovetheir starting condition. Some animals may benefit from theincreased calories available in captivity and be able to main-tain their weight. In other animals, however, ad libitum accessto food and limits to exercise may cause them to become obeseand face the myriad negative consequences of a high bodymass or body fat content (West and York, 1998). In a studyof domesticated budgerigars, birds were given ad libitum foodand confined to cages that limited exercise. High body massat the end of 28 days correlated with more DNA damage(Larcombe et al., 2015).

We visually summarized the patterns of weight changes inFig. 2. We graphed the total percent of studies that showedweight gain, weight loss or no change in weight at differenttime points after introduction to captivity. There were nostudies that recorded weight gain in the first day. Mostweight gain seems to be reported at 15–28 days of captiv-ity (38% of studies showed weight gain in that window).The percent of studies reporting weight loss decreased withincreasing captivity duration, reflecting the fact that manystudies show eventual regain of lost weight. This suggests that

for many species where weight was lost, it would eventuallybe regained.

It is possible that seasonal fluctuations in weight mayinterfere with the assumptions that weight gain or loss isdue to captivity. Captive ruffs and red knots have strong sea-sonal weight fluctuations in captivity associated with weightgain for migration and breeding (Piersma et al., 2000). Ifsemi-naturalistic conditions are maintained in captivity (forexample, if the animals are exposed to natural day length orare housed outdoors), then they may continue to experienceseasonal weight changes that are not due to overfeeding or tolong-term stressor exposure.

Changes in GCs during the adjustment tocaptivityOne of the most common variables to measure when assessingthe stress of captivity was GC concentrations. GC hormones(primarily cortisol in fish and most mammals; primarily cor-ticosterone in reptiles, birds, amphibians, and rodents) areproduced in the adrenal cortex, have multiple roles through-out the body, and can influence many other physiologicalsystems. Acute stressors cause a transitory increase in GCs,which is eventually brought down by negative feedback.Long-term stressor exposure frequently results in changesin GC regulation, although the part of the GC responseaffected (baseline concentrations, stress-induced concentra-tions, or negative feedback) and the direction of the changeare different in different species and circumstances (Dickensand Romero, 2013).

GCs can be assessed in several ways (Sheriff et al., 2011).The most common method is to measure circulating plasmaGCs by taking a blood sample. The sampling procedureitself can cause an increase in GCs, so researchers usually

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ated

mea

sure

s;m

ultip

letim

epoi

nts

Wei

ghtd

ecre

ased

over

5w

eeks

,in

crea

sed

thro

ugh

Wee

k20

(Bak

eret

al.,

1998

)∗

Tuco

-tuc

o(C

teno

mys

tala

rum

)Re

peat

edm

easu

res;

mul

tiple

timep

oint

sW

eigh

tlos

son

Day

s10

and

20,r

egai

ned

byD

ay30

(Ver

aet

al.,

2011

)∗

Bird

sW

hite

-cro

wne

dsp

arro

w(Z

onot

richi

ale

ucop

hrys

)Re

peat

edm

easu

res;

mul

tiple

timep

oint

sW

eigh

tlos

sat

Day

1,in

crea

sed

thro

ugh

day

14

(Win

gfiel

det

al.,

1982

)∗

Gre

enfin

ch(C

hlor

isch

loris

)Ca

ptiv

evs

free

-livi

ngpo

pula

tion

Bird

slig

hter

at1

mon

th,h

eavi

erth

anw

ildat

2m

onth

s

(Sep

pet

al.,

2010

)∗

Hou

sesp

arro

w(P

asse

rdo

mes

ticus

)Re

peat

edm

easu

res;

mul

tiple

timep

oint

sW

eigh

tlos

son

Day

s11

–25,

rega

ined

byda

y35

(Fis

cher

etal

.,20

18)∗

Chuk

arpa

rtrid

ge(A

lect

oris

chuk

ar)

Repe

ated

mea

sure

s;m

ultip

letim

epoi

nts

Wei

ghtl

oss

atD

ay1,

part

ially

rega

ined

at5

and

9da

ys

(Dic

kens

etal

.,20

09b)

∗

Fish

Skip

jack

tuna

(Kat

suw

onus

pela

mus

)Re

peat

edm

easu

res;

mul

tiple

timep

oint

sW

eigh

tlos

sat

Day

2,re

gain

edat

20da

ys(B

ourk

eet

al.,

1987

)

Chuk

arpa

rtrid

ge(A

lect

oris

chuk

ar)

Repe

ated

mea

sure

s;m

ultip

letim

epoi

nts

Wei

ghtl

oss

atD

ay1,

part

ially

rega

ined

at5

and

9da

ys

(Dic

kens

etal

.,20

09b)

∗

Fish

Skip

jack

tuna

(Kat

suw

onus

pela

mus

)Re

peat

edm

easu

res;

mul

tiple

timep

oint

sW

eigh

tlos

sat

Day

2,re

gain

edat

20da

ys(B

ourk

eet

al.,

1987

)

1N

oat

-cap

ture

valu

es—

first

mea

sure

dat

2m

onth

s.2

Low

sam

ple

size

sat

each

time

poin

t.3

Capt

ive

pups

wer

ere

habi

litat

edaf

terr

escu

e.4

Slig

htw

eigh

tlos

sfr

omD

ay10

toD

ay60

.5

Fem

ales

did

notr

each

atca

ptur

ew

eigh

t,bu

tall

spon

tane

ousl

yab

orte

dor

gave

birt

h.∗ D

ata

from

this

pape

rwer

eus

edto

gene

rate

Fig.

2.

..........................................................................................................................................................

8

Dow



ber 2022


try to acquire the first sample as quickly as possible—within3 minutes of capture or disturbance is generally considered agood guideline (Romero and Reed, 2005). In many studies,it was not possible for the researchers to meet this stan-dard because of the difficulty of capturing and bleeding theanimals. In addition, some papers were written before the3-minute standard had been established. It is also possibleto assess GCs through other means. Fecal samples can becollected to measure metabolized GCs. Fecal samples providean integrated profile of GC secretion over several hours toseveral days, depending upon the species, and reflect bothbaseline GCs and acute stress events (Wasser et al., 2000).Fecal sampling is convenient for many species when rapidcapture and blood sampling is impractical. If the first fecalsample is collected soon after capture, it will not reflect thestress of captivity and may be considered a good free-livingreference. Some researchers also used urinary GC metabolites,particularly in amphibian species, where animals could be leftalone in a container of water from which excreted steroidswere measured.

The initial capture and handling of wild animals isexpected to cause an increase in circulating GC levels (anacute stress response). While some researchers investigatedcaptivity-induced changes in the acute stress response itself(e.g. taking a plasma sample after a standardized 30-minuterestraint stress at capture and again after a period incaptivity), others incorporated the acute response to capturein the same analysis as longer-term captivity effects (e.g.taking a sample at 0, 2, 6, 18, 24, 48 and 72 hours postcapture). Because of the variety of different measures used, wefocused particularly on the captivity effects on baseline andintegrated GCs (Table 2). However, we will also discuss theeffects of captivity on the acute stress response and negativefeedback of GC production (Table 3). Some researcherslooked for the effects of captivity at different times of year—we do not include those studies in our calculations or inTables 2 and 3 (see Section 9).

Captivity does not influence GCs in all species. In 17%(10 of 59) studies, there was no recorded difference in GCsduring or after the captivity period compared to free-livinglevels. In most studies, however, captivity caused a change inbaseline or integrated GCs. In 42% of studies (25 of 59), wildanimals had increased GCs at the end of the capture periodcompared to concentrations in free-living animals (periodsof 3 days to several years). Elevated GCs are traditionallyinterpreted as an indication that animals are chronicallystressed. Experimentally induced chronic stress can often leadto elevated baseline GCs, although this is by no means auniversal response (Dickens and Romero, 2013). Adrenalhypertrophy may be an underlying mechanism explaining thelong-term elevation of GCs. For example, long-term captivityled to increased adrenal mass in African green monkeys(Suleman et al., 2004) and mouse lemurs (Perret, 1982).In nine-banded armadillos, 6 months of captivity (but not3 months) caused adrenal changes similar to those aftera harsh winter (Rideout et al., 1985) and in herring gulls

28 days of captivity led to adrenal lesions (Hoffman andLeighton, 1985).

However, many studies that reported elevated GC concen-trations at the end of the captivity period may eventuallyhave shown decreased GCs had the study been carried outfor longer. For example, house sparrows had elevated base-line GCs after 1–7 days in captivity (Kuhlman and Martin,2010; Lattin et al., 2012; Fischer and Romero, 2016). Butwhen captive house sparrows were sampled repeatedly over6 weeks of captivity, the high baseline GCs seen at Day 7 weredramatically reduced over Days 11–42 and approached at-capture concentrations in one study (Fischer et al., 2018), butdid not decrease in another study (Love et al., 2017).

The duration of captivity in the studies we collected wasquite variable, ranging from 3 days to several years. Toconsolidate the patterns from multiple studies with differ-ent sampling times, we graphed the percent of studies withelevated GCs (relative to free-living levels) against captivityduration (Fig. 3). We expected the percent of studies withelevated GCs to decrease as captivity duration increased (asshown in Fig. 1C and D). This pattern would indicate anadjustment to captivity conditions and is a typical a prioriprediction in the literature. However, we found that 45%(5 of 11) of species continued to have elevated GCs after3 months or more of captivity. This suggests that for manyspecies, there is never a complete adjustment to captivity. It isalso possible that a publication bias exists in the papers wecollected. When researchers did not see a difference betweenlong-term captives and free-living animals, they may havebeen less likely to publish, or perhaps included those resultsin other studies that did not appear in our literature searches.It is interesting to note that the fewest studies reportedelevated GCs at around two weeks post captivity, the amountof time that many researchers allow for their study speciesto become acclimated to laboratory conditions (e.g. Davieset al., 2013; Lattin and Romero, 2014; McCormick et al.,2015).

The analysis in Fig. 3 contains data collected from manydifferent taxa, study designs, etc. A more informative method-ology to investigate how GCs change over time in captivity isto compare multiple timepoints within the same experiment.We found 38 studies that used repeated sampling. Researcherseither repeatedly sampled individuals or captured many sub-jects at once and sampled them after different captivity dura-tions. In study designs with repeated sampling, 42% of studies(16 of 38) showed an early increase in GCs followed bya decrease back to free-living levels (e.g. Fig. 1C and D, thea priori prediction for GC adjustment to captivity). Of theremaining studies, 32% (12 of 38) matched the pattern inFig. 3 with no decrease in GC concentrations over time, 13%(5 of 38) showed decreased GC concentrations in captivityand 11% (4 of 38) reported no change in GCs whatsoever.When the expected peak and fall of GCs was observed, thetimescale of adjustment to captivity varied. Baseline GCsin mouse lemurs returned to at-capture levels by Day 5

..........................................................................................................................................................

9

Dow



ber 2022


Tabl

e2:

Patt

erns

ofch

ange

inba

selin

ean

din

tegr

ated

GCs

whe

nw

ildan

imal

sar

ebr

ough

tint

oca

ptiv

ity(t

his

tabl

edo

esno

tinc

lude

stud

ies

whe

reth

epa

tter

nw

asdi

ffere

ntin

diffe

rent

seas

ons—

thos

est

udie

sm

aybe

foun

din

Tabl

e6)

GC

Patt

ern

duri

ngad

just

men

tto

capt

ivit

y

Spec

ies

Stud

yde

sign

Tim

efra

me

How

wer

efr

ee-li

ving

GCs

esta

blis

hed?

Sam

ple

type

Cita

tion

No

effec

ton

GCs

over

capt

ivity

perio

d

Mam

mal

sD

egu

(Oct

odon

degu

s)Ca

ptiv

evs

free

-livi

ngpo

pula

tions

>1

year

Free

-livi

ngpo

pula

tion

Plas

ma

(<2

min

)(Q

uisp

eet

al.,

2014

)∗

Brus

htai

lpos

sum

s(T

richo

suru

svo

lpec

ula)

(♂on

ly)

Repe

ated

mea

sure

s;m

ultip

letim

epoi

nts

20w

eeks

Non

e—fir

stsa

mpl

eat

wee

k1

ofca

ptiv

ityPl

asm

a(<

5m

in)

(Bak

eret

al.,

1998

)

Brus

htai

lpos

sum

s(T

richo

suru

svo

lpec

ula)

(♂)Re

peat

edm

easu

res;

mul

tiple

timep

oint

sU

pto

8w

eeks

Non

e—un

clea

rw

hen

first

sam

ple

was

obta

ined

Plas

ma

(tim

eno

tgiv

en)

(Beg

get

al.,

2004

)

Har

bors

eal(

Phoc

avi

tulin

a)(ju

veni

le)

Capt

ive

vsfr

ee-li

ving

popu

latio

ns>

4w

eeks

Free

-livi

ngan

imal

sPl

asm

a(w

ild:6

0m

inca

ptiv

e:<

10m

in)

(Tru

mbl

eet

al.,

2013

)∗

Tuco

-tuc

o(C

teno

mys

tala

rum

)1Re

peat

edm

easu

res;

mul

tiple

timep

oint

s30

days

At-

capt

ure

mea

sure

Plas

ma

(<3

min

)(V

era

etal

.,20

11)∗

Bird

sEu

rope

anst

arlin

g(S

turn

usvu

lgar

is)Re

peat

edm

easu

res;

pre-

vspo

st-

capt

ivity

4w

eeks

+Fe

athe

rgro

wn

inth

ew

ildFe

athe

rs(F

isch

eret

al.,

2017

)

Wes

tern

scre

ech

owl

(Otu

sken

nico

ttii)

Capt

ive

vsfr

ee-li

ving

popu

latio

ns>

1m

onth

Free

-livi

ngan

imal

sPl

asm

a(<

5m

in)

(Duf

tyan

dBe

lthoff

,19

97)∗

Hou

sesp

arro

w(P

asse

rdom

estic

us)

Mul

tiple

timep

oint

s;di

ffere

ntin

divi

dual

sU

pto

4w

eeks

Free

-livi

ngan

imal

sPl

asm

a(<

3m

in)

(Mar

tinet

al.,

2011

)∗

Rept

iles

Tuat

ara

(Sph

enod

onpu

ncta

tus)

(♂on

ly)

Capt

ive

vsfr

ee-li

ving

popu

latio

nsU

nkno

wn

Free

-livi

ngpo

pula

tion

Plas

ma

(<20

min

)(T

yrre

llan

dCr

ee,

1994

)

Kutu

m(R

utilu

sfris

iiku

tum

)Ca

ptiv

evs

free

-livi

ngpo

pula

tions

3da

ysFr

ee-li

ving

popu

latio

nPl

asm

a(<

3m

in)

(Nik

ooet

al.,

2010

)∗

GCs

elev

ated

inca

ptiv

ityM

amm

als

Cana

daly

nx(L

ynx

cana

dens

is)2

Capt

ive

vsfr

ee-li

ving

popu

latio

nsLo

ngte

rm(u

nkno

wn)

3Fr

ee-li

ving

popu

latio

nFG

Ms

(Fan

son

etal

.,20

12)∗

Spid

erm

onke

y(A

tele

sgeo

ffroy

iyu

cata

nens

is)

Capt

ive

vsfr

ee-li

ving

popu

latio

nsLo

ngte

rm(u

nkno

wn)

2Fr

ee-li

ving

popu

latio

nFG

Ms

(Ran

gel-N

egrin

etal

.,20

09)∗

Afr

ican

wild

dog

(Lyc

aon

pict

us)

Capt

ive

vsfr

ee-li

ving

popu

latio

nsLo

ngte

rm(u

nkno

wn)

2Fr

ee-li

ving

popu

latio

nFG

Ms

(Van

derW

eyde

etal

.,20

16)∗

(Con

tinue

d)

..........................................................................................................................................................

10

Dow



ber 2022


Tabl

e2:

Cont

inua

tion

GC

Patt

ern

duri

ngad

just

men

tto

capt

ivit

y

Spec

ies

Stud

yde

sign

Tim

efra

me

How

wer

efr

ee-li

ving

GCs

esta

blis

hed?

Sam

ple

type

Cita

tion

Gre

vy’s

zebr

a(E

quus

grev

yi)

Repe

ated

mea

sure

s;m

ultip

letim

epoi

nts

6w

eeks

At-

capt

ure

sam

ple;

free

-livi

ngpo

pula

tion

FGM

s(F

ranc

esch

inie

tal.,

2008

)∗

Whi

terh

inos

(Cer

atot

heriu

msi

mum

)

Repe

ated

mea

sure

s;m

ultip

letim

epoi

nts

75da

ysA

t-ca

ptur

esa

mpl

eFG

Ms

(Lin

klat

eret

al.,

2010

)∗

Bird

sCu

rve-

bille

dth

rash

er(T

oxos

tom

acu

rver

ostr

e)

Repe

ated

mea

sure

s;m

ultip

letim

epoi

nts

80da

ysA

t-ca

ptur

esa

mpl

esPl

asm

a(<

3m

in)

(Fok

idis

etal

.,20

11)∗

Whi

te-c

row

ned

spar

row

(Zon

otric

hia

leuc

ophr

ys)

Capt

ive

vsfr

ee-li

ving

popu

latio

ns35

days

Free

-livi

ngpo

pula

tion

Plas

ma

(<1

min

)(M

arra

etal

.,19

95)∗

Whi

te-t

hroa

ted

spar

row

(Zon

otric

hia

albi

colli

s)

Capt

ive

vsfr

ee-li

ving

popu

latio

ns35

days

Free

-livi

ngpo

pula

tion

Plas

ma

(<1

min

)(M

arra

etal

.,19

95)∗

Blac

kbird

s(T

urdu

sm

erul

a)Re

peat

edm

easu

res;

pre-

vspo

st-c

aptiv

ity22

days

At-

capt

ure

sam

ple

Plas

ma

(<3

min

)(A

dam

set

al.,

2011

)∗

Hou

sesp

arro

w(P

asse

rdom

estic

us)

Repe

ated

mea

sure

s;m

ultip

letim

epoi

nts

7da

ysA

t-ca

ptur

esa

mpl

ePl

asm

a(<

3m

in)

(Fis

cher

and

Rom

ero,

2016

)∗

Hou

sesp

arro

w(P

asse

rdom

estic

us)

Repe

ated

mea

sure

s;m

ultip

letim

epoi

nts

7da

ysA

t-ca

ptur

esa

mpl

ePl

asm

a(<

3m

in)

(Fis

cher

etal

.,20

18)∗

Hou

sesp

arro

w(P

asse

rdom

estic

us)

Repe

ated

mea

sure

s;pr

e-vs

post

-cap

tivity

(mul

tiple

seas

ons)

5da

ysA

t-ca

ptur

esa

mpl

ePl

asm

a(<

3m

in)

(Lat

tinet

al.,

2012

)∗

Hou

sesp

arro

w(P

asse

rdom

estic

us)

Repe

ated

mea

sure

s;m

ultip

letim

epoi

nts

66da

ysA

t-ca

ptur

esa

mpl

ePl

asm

a(<

3m

in)

(Lov

eet

al.,

2017

)∗

Hou

sesp

arro

w(P

asse

rdom

estic

us)

Repe

ated

mea

sure

s;m

ultip

letim

epoi

nts

24da

ysA

t-ca

ptur

esa

mpl

ePl

asm

a(<

3m

in)

(Gor

mal

lyet

al.,

2019

)∗

Sout

hern

pied

babb

lers

(Tur

doid

esbi

colo

r)

Capt

ive

vsfr

ee-li

ving

popu

latio

ns5

days

Free

-livi

ngpo

pula

tion

FGM

s(J

epse

net

al.,

2019

)∗

Rept

iles

Tuat

ara

(Sph

enod

onpu

ncta

tus)

(♀onl

y)Ca

ptiv

evs

free

-livi

ngpo

pula

tions

Unk

now

nFr

ee-li

ving

popu

latio

nPl

asm

a(<

20m

in)

(Tyr

rell

and

Cree

,19

94)∗

(Con

tinue

d)

..........................................................................................................................................................

11

Dow



ber 2022


Tabl

e2:

Cont

inau

tion

GC

Patt

ern

duri

ngad

just

men

tto

capt

ivit

y

Spec

ies

Stud

yde

sign

Tim

efra

me

How

wer

efr

ee-li

ving

GCs

esta

blis

hed?

Sam

ple

type

Cita

tion

Gar

ters

nake

(Tha

mno

phis

eleg

ans)

Repe

ated

mea

sure

s;m

ultip

letim

epoi

nts

4m

onth

sA

t-ca

ptur

esa

mpl

e;fr

ee-li

ving

popu

latio

n

Plas

ma

(<10

min

)4(S

park

man

etal

.,20

14)∗

Tree

lizar

d(U

rosa

urus

orna

tus)

Mul

tiple

timep

oint

s;di

ffere

ntin

divi

dual

sU

pto

3w

eeks

At-

capt

ure

sam

ples

Plas

ma

(<1

min

)(M

oore

etal

.,19

91)∗

Wat

ersn

ake

(Ner

odia

sipe

don)

Repe

ated

mea

sure

s;pr

e-vs

post

-cap

tivity

5–8

days

At-

capt

ure

sam

ples

Plas

ma

(<5

min

)(S

ykes

and

Kluk

owsk

i,20

09)∗

Brow

ntr

eesn

ake

(Boi

gairr

egul

aris

)M

ultip

letim

epoi

nts;

diffe

rent

indi

vidu

als

3da

ysFr

ee-li

ving

popu

latio

nPl

asm

a(<

8m

in)

(Mat

hies

etal

.,20

01)∗

Am

phib

ians

Curu

ruto

ad(R

hine

llaic

teric

a)Re

peat

edm

easu

res;

pre-

vspo

st-c

aptiv

ity3

mon

ths

At-

capt

ure

sam

ple

Plas

ma

(<3

min

)(d

eA

ssis

etal

.,20

15)∗

Toad

(Rhi

nella

schn

eide

ri)Re

peat

edm

easu

res;

pre-

vspo

st-c

aptiv

ity60

days

At-

capt

ure

sam

ple

Plas

ma

(<3

min

)(T

iton

etal

.,20

17)∗

Gre

enfr

og(R

ana

escu

lent

a)Re

peat

edm

easu

res;

mul

tiple

timep

oint

s(m

ultip

lese

ason

s)

3da

ysA

t-ca

ptur

esa

mpl

ePl

asm

a(<

5m

in)

(Zer

anie

tal.,

1991

)∗

Fish

Cora

lree

ffish

(Hem

igym

nus

mel

apte

rus)

Capt

ive

vsfr

ee-li

ving

popu

latio

ns2.

5m

onth

sFr

ee-li

ving

popu

latio

nPl

asm

a(<

6m

in)

(Gru

tter

and

Pank

hurs

t,20

00)∗

Wed

geso

le(D

icol

ogog

loss

acu

neat

e)(ju

veni

le)

Mul

tiple

timep

oint

s;di

ffere

ntin

divi

dual

s45

days

At-

hatc

hing

sam

ples

Who

le-b

ody

(tim

eno

tgi

ven)

(Her

rera

etal

.,20

16)∗

GCs

incr

ease

at-c

aptu

re,t

hen

decr

ease

toap

proa

chw

ildba

selin

e

Mam

mal

sBe

luga

wha

le(D

elph

inap

teru

sle

ucas

)

Repe

ated

mea

sure

s;m

ultip

letim

epoi

nts

Peak

:1da

yap

proa

chfr

ee-li

ving

by4

days

At-

capt

ure

sam

ple

and

free

-livi

ngpo

pula

tion

Plas

ma

(tim

eno

tgiv

en)

(StA

ubin

and

Ger

aci,

1989

)∗

Chac

ma

babo

on(P

apio

ursi

nus)

Repe

ated

mea

sure

s;m

ultip

letim

epoi

nts

Peak

:4w

eeks

appr

oach

long

-ter

mca

ptiv

esby

7w

eeks

Non

e—us

edlo

ngte

rmca

ptiv

esas

base

line.

Plas

ma

(tim

eno

tgiv

en)

(Ste

yn,1

975)

(Con

tinue

d)

..........................................................................................................................................................

12

Dow



ber 2022


Tabl

e2:

Cont

inua

tion

GC

Patt

ern

duri

ngad

just

men

tto

capt

ivit

y

Spec

ies

Stud

yde

sign

Tim

efra

me

How

wer

efr

ee-li

ving

GCs

esta

blis

hed?

Sam

ple

type

Cita

tion

Afr

ican

gree

nm

onke

y(C

erco

pith

ecus

aeth

iops

)

Mul

tiple

timep

oint

s;di

ffere

ntin

divi

dual

sPe

ak:1

day

appr

oach

free

-livi

ngby

2da

ys

Free

-livi

ngpo

pula

tion

Plas

ma

(tim

eno

tgiv

en)

(Sul

eman

etal

.,20

04)∗

Mou

sele

mur

(Mic

roce

busm

urin

us)

Repe

ated

mea

sure

s;m

ultip

letim

epoi

nts

Peak

:2da

ysap

proa

chfr

ee-li

ving

by4

days

At-

capt

ure

sam

ple

FGM

s(H

amal

aine

net

al.,

2014

)∗

Rich

ards

on’s

grou

ndsq

uirr

el(U

roci

tellu

sric

hard

soni

i)

Repe

ated

mea

sure

s;m

ultip

letim

epoi

nts

Peak

:3–5

days

appr

oach

free

-livi

ngby

6da

ys

At-

capt

ure

sam

ple

FGM

s(H

are

etal

.,20

14)∗

Bott

leno

sedo

lphi

n(T

ursi

opst

runc

atus

)Re

peat

edm

easu

res;

mul

tiple

timep

oint

sPe

ak:1

day

appr

oach

long

-ter

mca

ptiv

eby

2w

eeks

Long

-ter

mca

ptiv

esPl

asm

a(t

ime

notg

iven

)(O

rlov

etal

.,19

91)

Bird

sH

ouse

spar

row

(Pas

serd

omes

ticus

)Re

peat

edm

easu

res;

mul

tiple

timep

oint

sPe

ak:D

ay7

appr

oach

free

-livi

ngby

Day

11

At-

capt

ure

sam

ple

Plas

ma

(<3

min

)(F

isch

eret

al.,

2018

)∗

Hou

sesp

arro

w(P

asse

rdom

estic

us)

Repe

ated

mea

sure

s;m

ultip

letim

epoi

nts

Peak

:Day

s1–

2ap

proa

chfr

ee-li

ving

by1

mon

th

At-

capt

ure

sam

ple

Plas

ma

(<3

min

)(K

uhlm

anan

dM

artin

,201

0)∗

Whi

te-c

row

ned

spar

row

(Zon

otric

hia

leuc

ophr

ys)

Repe

ated

mea

sure

s;m

ultip

letim

epoi

nts

Peak

:Day

s1–

2ap

proa

chfr

ee-li

ving

byD

ay14

At-

capt

ure

sam

ple

Plas

ma

(tim

eno

tgiv

en)

(Win

gfiel

det

al.,

1982

)∗

Rept

iles

Skin

k(E

gern

iaw

hitii

)Re

peat

edm

easu

res;

mul

tiple

timep

oint

sPe

ak:

1da

y–1

wee

kap

proa

chfr

ee-li

ving

by4

wee

ks

At-

capt

ure

sam

ple

Plas

ma

(<1

min

)(J

ones

and

Bell,

2004

)∗

(Con

tinue

d)

..........................................................................................................................................................

13

Dow



ber 2022


Tabl

e2:

Cont

inua

tion

GC

Patt

ern

duri

ngad

just

men

tto

capt

ivit

y

Spec

ies

Stud

yde

sign

Tim

efra

me

How

wer

efr

ee-li

ving

GCs

esta

blis

hed?

Sam

ple

type

Cita

tion

Am

phib

ians

Wat

erfr

og(R

ana

escu

lent

a)M

ultip

letim

epoi

nts;

diffe

rent

indi

vidu

als

Peak

:Day

1ap

proa

chfr

ee-li

ving

byD

ay7

Free

-livi

ngpo

pula

tions

Plas

ma

(<3

min

)(G

obbe

ttia

ndZe

rani

,199

6)∗

Cane

toad

(Rhi

nella

mar

ina)

Repe

ated

mea

sure

s;m

ultip

letim

epoi

nts

Peak

:Day

5ap

proa

chfr

ee-li

ving

byD

ay12

At-

capt

ure

sam

ple

Urin

e(N

aray

anet

al.,

2011

)∗

Cane

toad

(Rhi

nella

mar

ina)

Repe

ated

mea

sure

s;m

ultip

letim

epoi

nts

Peak

:Day

4ap

proa

chfr

ee-li

ving

byD

ay14

At-

capt

ure

sam

ple

Urin

e(N

aray

anet

al.,

2012

)∗

Fijia

ngr

ound

frog

(Pla

tym

antis

vitia

na)

Repe

ated

mea

sure

s;m

ultip

letim

epoi

nts

Peak

:Day

5ap

proa

chfr

ee-li

ving

byD

ay25

At-

capt

ure

sam

ple

Urin

e(N

aray

anan

dH

ero,

2011

)∗

Fish

Flou

nder

(Par

alic

hthy

sor

bign

yanu

s)

Mul

tiple

timep

oint

s;di

ffere

ntin

divi

dual

sPe

ak:1

hour

appr

oach

free

-livi

ngby

Day

1

Free

-livi

ngan

imal

sPl

asm

a(<

7m

in)

(Bol

asin

a,20

11)∗

Kaha

wai

(Arr

ipis

trut

ta)

Mul

tiple

timep

oint

s;di

ffere

ntin

divi

dual

sPe

ak:

2–3

hour

sap

proa

chfr

ee-li

ving

byD

ay3

Free

-livi

ngan

imal

sPl

asm

a(<

4m

in)

(Dav

idso

net

al.,

1997

)∗

GCs

low

erin

capt

ivity

Mam

mal

sH

arbo

rpor

pois

e(P

hoco

ena

phoc

oena

)Ca

ptiv

evs

free

-livi

ngpo

pula

tions

Long

term

(unk

now

n)Fr

ee-li

ving

popu

latio

nPl

asm

a(t

ime

notg

iven

)(S

iebe

rtet

al.,

2011

)∗

Gilb

ert’s

poto

roo

(Pot

orou

sgilb

ertii

)Ca

ptiv

evs

free

-livi

ngpo

pula

tions

Long

term

(unk

now

n)Fr

ee-li

ving

popu

latio

nFG

Ms

(Ste

ad-R

icha

rdso

net

al.,

2010

)∗

Har

bors

eal(

Phoc

avi

tulin

a)Re

peat

edm

easu

res;

mul

tiple

timep

oint

sLo

ngte

rm(u

nkno

wn)

Free

-livi

ngpo

pula

tion

Plas

ma

(tim

eno

tgiv

en)

(Gar

dine

rand

Hal

l,19

97)∗

Blac

krh

ino

(Dic

eros

bico

rnis

)5Re

peat

edm

easu

res;

mul

tiple

timep

oint

s60

days

At-

capt

ure

sam

ple

FGM

s(L

inkl

ater

etal

.,20

10)∗

(Con

tinue

d)

..........................................................................................................................................................

14

Dow



ber 2022


Tabl

e2:

Cont

inua

tion

GC

Patt

ern

duri

ngad

just

men

tto

capt

ivit

y

Spec

ies

Stud

yde

sign

Tim

efra

me

How

wer

efr

ee-li

ving

GCs

esta

blis

hed?

Sam

ple

type

Cita

tion

Whi

tew

hale

(Del

phin

apte

rus

leuc

as)

Repe

ated

mea

sure

s;m

ultip

letim

epoi

nts

11da

ysLo

ng-t

erm

capt

ives

Plas

ma

(tim

eno

tgiv

en)

(Orlo

vet

al.,

1991

)

Bird

sEu

rope

anst

arlin

g(S

turn

usvu

lgar

is)Ca

ptiv

evs

free

-livi

ngpo

pula

tion

Unk

now

nFr

ee-li

ving

popu

latio

nFG

Ms

(Cyr

and

Rom

ero,

2008

)

Chuk

arpa

rtrid

ge(A

lect

oris

chuk

ar)

Repe

ated

mea

sure

s;m

ultip

letim

epoi

nts

9da

ysA

t-ca

ptur

esa

mpl

ePl

asm

a(<

3m

in)

(Dic

kens

etal

.,20

09a)

∗

Am

phib

ians

Toad

(Rhi

nella

icte

rica)

Capt

ive

vsfr

ee-li

ving

popu

latio

n,m

ultip

letim

epoi

nts6

Dec

reas

edfr

omD

ays

30to

60

Free

-livi

ngpo

pula

tion

Plas

ma

(<3

min

)(T

iton

etal

.,20

18)∗

Hig

hin

itial

GCs

decr

ease

over

capt

ure

perio

d

Mam

mal

sRh

esus

mac

aque

s(M

acac

am

ulat

ta)

Repe

ated

mea

sure

s;m

ultip

letim

epoi

nts

Dec

reas

edfr

omD

ay1

to1

year

Non

e—fir

stsa

mpl

eaf

teru

nkno

wn

time

intr

ap.

Plas

ma

(<50

min

)(L

illy

etal

.,19

99)

Brus

htai

lpos

sum

s(T

richo

suru

svo

lpec

ula)

(♀onl

y)

Repe

ated

mea

sure

s;m

ultip

letim

epoi

nts

Dec

reas

edfr

omW

eek

1to

20

Non

e—fir

stsa

mpl

eat

Wee

k1

ofca

ptiv

ityPl

asm

a(<

5m

in)

(Bak

eret

al.,

1998

)

Mea

dow

vole

(Mic

rotu

spe

nnsy

lvan

icus

)

Mul

tiple

timep

oint

s;di

ffere

ntin

divi

dual

sD

ecre

ased

from

Day

1to

Day

70

Non

e—fir

stsa

mpl

eat

Day

1Pl

asm

a(<

1m

in)

(Ols

enan

dSe

ablo

om,1

973)

Vicu

ñas

(Vic

ugna

vicu

gna)

Repe

ated

mea

sure

s;m

ultip

letim

epoi

nts

Dec

reas

edfr

omat

-cap

ture

toD

ay12

Non

e—fir

stsa

mpl

eaf

ters

tres

sful

capt

ure

(tim

eno

tgi

ven)

Plas

ma

(tim

eno

tgiv

en)

(Bon

acic

and

Mac

dona

ld,2

003)

Eura

sian

otte

r(Lu

tra

lutr

a)7

Repe

ated

mea

sure

s;m

ultip

letim

epoi

nts

Dec

reas

edfr

omD

ays

2–5

toD

ays

5–10

Non

e—fir

stsa

mpl

eat

Day

s2–

5Pl

asm

a(t

ime

notg

iven

)(F

erna

ndez

-Mor

anet

al.,

2004

)

Bird

sRe

dkn

ot(C

alid

risca

nutu

s)Re

peat

edm

easu

res;

mul

tiple

timep

oint

sD

ecre

ased

from

first

sam

ple

to2

year

s

Non

e—fir

stsa

mpl

eat

day

70Pl

asm

a(3

–38

min

)(P

iers

ma

and

Ram

enof

sky,

1998

)

(Con

tinue

d)

..........................................................................................................................................................

15

Dow



ber 2022


Tabl

e2:

Cont

inua

tion

GC

Patt

ern

duri

ngad

just

men

tto

capt

ivit

y

Spec

ies

Stud

yde

sign

Tim

efra

me

How

wer

efr

ee-li

ving

GCs

esta

blis

hed?

Sam

ple

type

Cita

tion

Fish

Red

gurn

ard

(Che

lidon

icht

hys

kum

u)

Repe

ated

mea

sure

s;pr

e-vs

post

-cap

tivity

(diff

eren

tdur

atio

ns)

Dec

reas

edfr

omfir

stsa

mpl

eto

1da

y

Non

e—fir

stsa

mpl

eaf

terl

ong

line

capt

ure

Plas

ma

(<2

min

)(C

lear

wat

er,1

997)

Snap

per(

Pagr

usau

ratu

s)M

ultip

letim

epoi

nts;

diffe

rent

indi

vidu

als

Dec

reas

edfo

rmat

-cap

ture

toD

ay2

Non

e—fir

stsa

mpl

eaf

terl

ong

line

capt

ure

Plas

ma

(<10

min

)(P

ankh

urst

and

Shar

ples

,199

2)

Sard

ine

(Sar

dina

pilc

hard

us)

Mul

tiple

timep

oint

s;di

ffere

ntin

divi

dual

sD

ecre

ased

from

at-c

aptu

reto

Day

2

Non

e—fir

stsa

mpl

eaf

ters

eine

capt

ure

Plas

ma

(∼3

min

)(M

arca

loet

al.,

2008

)

1Co

rtis

olre

sults

only

.2

No

diffe

renc

ein

GCs

infe

mal

espr

e-br

eedi

ng—

GCs

elev

ated

inbo

thse

xes

durin

gbr

eedi

ngse

ason

.3

Capt

ive

popu

latio

nm

ayin

clud

eso

me

capt

ive-

rais

edin

divi

dual

s.4

Bloo

dsa

mpl

ing

took

long

erin

som

esa

mpl

es.

5G

Csp

ike

inm

any

anim

als

durin

gfir

st2

wee

ks,b

utth

endr

ops

wel

lbel

owat

capt

ure

leve

ls.

6G

Csin

crea

sed

inno

n-ca

lling

toad

s,bu

tsam

ple

size

slo

w.

7So

me

anim

als

trea

ted

with

long

-act

ing

neur

olep

tic,w

hich

had

noeff

ecto

nG

Cle

vels

,so

valu

esw

ere

pool

ed.

∗ Dat

afr

omth

ispa

pera

rein

corp

orat

edin

toFi

g.3.

..........................................................................................................................................................

16

Dow



ber 2022


Tabl

e3:

Patt

erns

ofch

ange

inst

ress

-indu

ced

GCs

and

nega

tive

feed

back

with

capt

ivity

inw

ildan

imal

s

GC

patt

ern

durin

gad

just

men

tto

capt

ivity

Spec

ies

Stud

yde

sign

Tim

efra

me

How

was

free

-livi

ngG

Cses

tabl

ishe

d?

Sam

ple

type

Cita

tion

No

chan

gein

acut

est

ress

-indu

ced

GCs

over

capt

ivity

perio

d

Mam

mal

sTu

co-t

uco

(Cte

nom

ysta

laru

m)

Capt

ive

vsfr

ee-li

ving

popu

latio

ns

20da

ysFr

ee-li

ving

popu

latio

nPl

asm

a(3

0an

d60

min

)(V

era

etal

.,20

11)

Bird

sCu

rve-

bille

dth

rash

er(T

oxos

tom

acu

rver

ostr

e)

Repe

ated

mea

sure

s;m

ultip

letim

epoi

nts

80da

ysA

t-ca

ptur

esa

mpl

esPl

asm

a(3

0m

in)

(Fok

idis

etal

.,20

11)

Blac

kbird

s(T

urdu

smer

ula)

Repe

ated

mea

sure

s;pr

e-vs

post

-cap

tivity

22da

ysA

t-ca

ptur

esa

mpl

ePl

asm

a(3

0an

d60

min

)(A

dam

set

al.,

2011

)

Wes

tern

scre

ech

owl(

Otu

ske

nnic

ottii

)

Capt

ive

vsfr

ee-li

ving

popu

latio

ns

>1

mon

thFr

ee-li

ving

anim

als

Plas

ma

(6–1

0m

in)

(Duf

tyJr

and

Belth

off,1

997)

Hou

sesp

arro

w(P

asse

rdo

mes

ticus

)1

Repe

ated

mea

sure

s;pr

e-vs

post

-cap

tivity

5da

ysA

t-ca

ptur

esa

mpl

ePl

asm

a(3

0m

in)

(Lat

tinet

al.,

2012

)

Hou

sesp

arro

w(P

asse

rdo

mes

ticus

)

Mul

tiple

timep

oint

s;di

ffere

ntin

divi

dual

s

Up

to1

mon

thA

t-ca

ptur

esa

mpl

ePl

asm

a(6

0m

in)

(Kuh

lman

and

Mar

tin,2

010)

Hou

sesp

arro

w(P

asse

rdo

mes

ticus

)

Repe

ated

mea

sure

s;m

ultip

letim

epoi

nts

7da

ysA

t-ca

ptur

esa

mpl

ePl

asm

a(3

0m

in)

(Fis

cher

and

Rom

ero,

2016

)∗

Hou

sesp

arro

w(P

asse

rdo

mes

ticus

)

Repe

ated

mea

sure

s;m

ultip

letim

epoi

nts

7da

ysA

t-ca

ptur

esa

mpl

ePl

asm

a(3

0m

in)

(Fis

cher

etal

.,20

18)∗

Hou

sesp

arro

w(P

asse

rdo

mes

ticus

)

Repe

ated

mea

sure

s;m

ultip

letim

epoi

nts

66da

ysA

t-ca

ptur

esa

mpl

ePl

asm

a(3

0m

in)

(Lov

eet

al.,

2017

)

(Con

tinue

d)

..........................................................................................................................................................

17

Dow



ber 2022


Tabl

e3:

Cont

inua

tion

GC

patt

ern

durin

gad

just

men

tto

capt

ivity

Spec

ies

Stud

yde

sign

Tim

efra

me

How

was

free

-livi

ngG

Cses

tabl

ishe

d?

Sam

ple

type

Cita

tion

Whi

te-c

row

ned

spar

row

(Zon

otric

hia

leuc

ophr

ys)2

Repe

ated

mea

sure

s;m

ultip

letim

epoi

nts

Up

to1

year

Free

-livi

ngpo

pula

tion

Plas

ma

(<30

min

)(R

omer

oan

dW

ingfi

eld,

1999

)

Fish

Win

terfl

ound

er(P

seud

ople

u-ro

nect

esam

eric

anus

)

Repe

ated

mea

sure

s;m

ultip

letim

epoi

nts

Up

to1

year

Free

-livi

ngpo

pula

tion

Plas

ma

(60

min

)(P

lant

eet

al.,

2003

)

Acut

est

ress

-indu

ced

GCs

redu

ced

inca

ptiv

ity

Bird

sCh

ukar

part

ridge

(Ale

ctor

isch

ukar

)

Repe

ated

mea

sure

s;m

ultip

letim

epoi

nts

9da

ysA

t-ca

ptur

esa

mpl

ePl

asm

a(3

0m

in)

(Dic

kens

etal

.,20

09a)

Whi

te-c

row

ned

spar

row

(Zon

otric

hia

leuc

ophr

ys)3

Repe

ated

mea

sure

s;m

ultip

letim

epoi

nts

Up

to1

year

Free

-livi

ngpo

pula

tion

Plas

ma

(30

min

)(R

omer

oan

dW

ingfi

eld,

1999

)

Acut

est

ress

-indu

ced

GCs

incr

ease

din

capt

ivity

Mam

mal

sD

egu

(Oct

odon

degu

s)Ca

ptiv

evs

free

-livi

ngpo

pula

tions

>1

year

Free

-livi

ngpo

pula

tion

Plas

ma

(30

and

60m

in)

(Qui

spe

etal

.,20

14)

Bird

sW

hite

-cro

wne

dsp

arro

w(Z

onot

richi

ale

ucop

hrys

)4

Repe

ated

mea

sure

s;m

ultip

letim

epoi

nts

Up

to1

year

Free

-livi

ngpo

pula

tion

Plas

ma

(30

min

)(R

omer

oan

dW

ingfi

eld,

1999

)

Rept

iles

Wat

ersn

ake

(Ner

odia

sipe

don)

Repe

ated

mea

sure

s;pr

e-vs

post

-cap

tivity

5–8

days

At-

capt

ure

sam

ple

Plas

ma

(60

min

)(S

ykes

and

Kluk

owsk

i,20

09)

Am

phib

ians

East

ern

red-

spot

ted

new

t(N

otop

htha

lmus

virid

esce

ns)5

Repe

ated

mea

sure

s;m

ultip

letim

epoi

nts

>1

year

Free

-livi

ngpo

pula

tion

Plas

ma

(30

min

)(B

erne

reta

l.,20

13)

(Con

tinue

d)

..........................................................................................................................................................

18

Dow



ber 2022


Tabl

e3:

Cont

inua

tion

GC

patt

ern

durin

gad

just

men

tto

capt

ivity

Spec

ies

Stud

yde

sign

Tim

efra

me

How

was

free

-livi

ngG

Cses

tabl

ishe

d?

Sam

ple

type

Cita

tion

Neg

ativ

efe

edba

ckst

reng

thde

crea

sed

with

capt

ivity

,the

nin

crea

sed

Bird

sCh

ukar

part

ridge

(Ale

ctor

isch

ukar

)

Repe

ated

mea

sure

s;m

ultip

letim

epoi

nts

Neg

.fee

dbac

kre

duce

dat

Day

5;re

cove

red

atD

ay9

At-

capt

ure

sam

ple

Plas

ma

(90

min

afte

rDEX

)(D

icke

nset

al.,

2009

b)

Neg

ativ

efe

edba

ckst

reng

thin

crea

sed

with

capt

ivity

Bird

sH

ouse

spar

row

(Pas

ser

dom

estic

us)

Repe

ated

mea

sure

s;pr

e-vs

post

-cap

tivity

5da

ysA

t-ca

ptur

esa

mpl

ePl

asm

a90

min

afte

rDEX

)(L

attin

etal

.,20

12)

Neg

ativ

efe

edba

ckst

reng

thdi

dno

tch

ange

with

capt

ivity

Bird

sH

ouse

spar

row

(Pas

ser

dom

estic

us)

Repe

ated

mea

sure

s;m

ultip

letim

epoi

nts

66da

ysA

t-ca

ptur

esa

mpl

ePl

asm

a90

min

afte

rDEX

)(L

ove

etal

.,20

17)

1SI

GCs

low

erpo

stca

ptiv

ityin

early

win

ter,

butn

och

ange

durin

gan

yot

hert

ime

ofye

ar.

2O

utsi

deof

bree

ding

seas

onan

dm

olt.

3D

urin

gth

ebr

eedi

ngse

ason

.4

Dur

ing

the

post

-bre

edin

g/m

oltin

gse

ason

.5

SIG

Cshi

gher

post

capt

ivity

inpr

e-br

eedi

ngan

dbr

eedi

ngse

ason

,not

inw

inte

r.

..........................................................................................................................................................

19

Dow



ber 2022


(Hamalainen et al., 2014) while the Fijian ground frog hadelevated urinary GCs until Day 25 post capture (Narayan andHero, 2011).

In some studies with repeated measures designs, theresearchers did not or could not obtain a sample thatrepresented free-living animals. In these cases, the first samplecould not be acquired until minutes, hours or even daysafter capture. In all nine studies where this was the case (seeTable 2), initially high concentrations of GCs decreased overthe study period in at least some animals. This is consistentwith the pattern we expect for animals successfully adjustingto captivity: capture, handling and the initial transfer tocaptivity result in high GCs that decrease as the animaladjusts. For example, female brushtail possums were notsampled until days after their capture and transfer to captivity,but showed decreasing plasma GCs from week 1 to week 20of captivity (Baker et al., 1998).

These studies on baseline GCs together demonstrate apattern wherein approximately half of species appear toadjust to captivity. Although some species seem to take longerto acclimate to captive conditions than others, it appearsthat many species will eventually show a reduction in GCsafter an initial peak. We see this pattern across taxonomicgroups, in birds, fish, reptiles, amphibians and mammals.However, we should be careful to not interpret a reduction incirculating baseline GCs, fecal GC metabolites or urinary GCsas a complete adjustment to captivity or an elimination ofchronic stress. Even when baseline GCs have returned to free-living levels, other aspects of the animals’ physiologies maybe negatively impacted. For example, even though circulatingGCs were only elevated for 1 day in African green monkeys,adrenal mass was almost doubled after 45 days in captivity(Suleman et al., 2004). Similarly, while it is tempting to con-clude that elevated GCs are diagnostic of chronic stress, itshould be kept in mind that baseline GCs have many functionsin metabolism and energy use. A change of baseline GCs incaptivity could merely reflect a change in energy requirementsand not the physiological damage we associate with chronicstress. Furthermore, a reduction in GCs in captivity, as seen in14% of studies (8 of 59), could be interpreted as a reductionin allostatic load or as the exhaustion of adrenal capacity.

Impact of captivity on acute stress response andnegative feedback of GC production

Relatively few researchers have explicitly investigated theeffects of captivity on the acute GC stress response (seeTable 3). Of those that have, 65% (11 of 17) found no effectof captivity (captivity duration 5–80 days). The six studiesthat reported changes in stress-induced GCs showed changesin opposite directions. In two studies, stress-induced GCswere decreased in captivity, even though the captive periodsof 9 days (Dickens et al., 2009a) and 1 year (Romero andWingfield, 1999) were quite different. In contrast, stress-induced GCs were increased in captivity in four studies oversimilar time frames. Three studies had animals in captivity

for about a year (Romero and Wingfield, 1999; Berner et al.,2013; Quispe et al., 2014), with 5–8 days in the fourth study(Sykes and Klukowski, 2009).

The negative feedback of the GC response to stress, wherehigh GC levels lead to the inhibition of GC production, is veryimportant for the control of physiological stress (Vitouseket al., 2019). Although chronic stress has frequently beenfound to affect the negative feedback of GC production(Dickens and Romero, 2013), we found only three studiesthat explicitly measured negative feedback strength in animalsimmediately at capture and after a period of captivity. Ineach case, animals were injected with a synthetic GC (dexam-ethasone) after mounting a stress response to stimulate max-imum negative feedback. The strength of negative feedbackincreased slightly in house sparrows after 5 days of captivity(Lattin et al., 2012), but in the same species showed no changeafter 21, 42 or 66 days (Love et al., 2017). In contrast,negative feedback strength decreased after 5 days of captivityin chukar partridges but returned to its at-capture strengthby 9 days (Dickens et al., 2009b). This is an important aspectof stress physiology, one that is critical for the total amountof GC exposure, and warrants further study to determinewhether it is impacted by the stress of captivity in manyspecies.

Immune consequences of captivityStress has well-documented, but sometimes complex, effectson the immune system. In large part, these changes are due tothe acute or long-term effects of elevated GCs on leukocytepopulations. GCs can cause immune redistribution, movinglymphocytes out of the bloodstream and into the skin, spleenand lymph nodes, where they will be available in case ofa wound (Dhabhar and McEwen, 1997; Johnstone et al.,2012). GCs can also cause proliferation or mobilization ofneutrophils (most vertebrates) or heterophils (birds and somereptiles) (Dale et al., 1975; Gross and Siegel, 1983; Johnstoneet al., 2012). Together, these effects on leukocyte populationsresult in a change in the neutrophil or heterophil to lympho-cyte ratio (N or H:L ratio) (Dhabhar and McEwen, 1997;Johnstone et al., 2012). A change in the N or H:L ratio doesnot necessarily mean that an animal’s immune system is hypo-or hyperactive. Instead, this acts as another metric similar toGC secretion. A long-term increase in N or H:L ratio, like along-term increase in circulating GCs, can be an indicationthat an animal is suffering from chronic stress (Davis et al.,2008).

We summarized the 23 studies that reported leukocytecounts in Table 4. Although the N or H:L is a useful metric,in some studies the researchers chose to report total num-ber or percent of different leukocyte types without calcu-lating or performing statistics on the relative abundances ofneutrophils/heterophils and lymphocytes. In these cases, weinferred the direction (or presence) of change after captivityof the N or H:L ratio based on the changes in leukocyte

..........................................................................................................................................................

20

Dow



ber 2022


counts or percentages that were reported. In two studies,only the total number of leukocytes was reported withoutfurther subdivision of leukocyte types. In 48% of studies(10 of 21), N or H:L ratio was elevated at the end of themeasured captivity duration relative to its free-living value.29% of studies (6 of 21) documented no change in N or H:Lratio over the study period. N or H:L ratio was decreased in24% of studies (5 of 21). In one study (in the Fijian groundfrog), the N:L ratio was elevated for 15 days in captivity,but then returned to wild levels by Day 25, resulting in nooverall change (Narayan and Hero, 2011). Kuhlman andMartin (2010) further investigated leukocyte redistributionto the skin in house sparrows, comparing Day 1of captivityto Day 30. They concluded that the changes in H:L ratiowere not due to redistribution of leukocytes, at least in thisinstance. We summarized the overall patterns of N or H:Lratio compared to captivity duration in Fig. 4. The number ofstudies reporting an increase in N or H:L ratio decreases withcaptivity duration. This suggests that many or most species doadjust to captivity, and an initially high N or H:L ratio maydecrease given sufficient time.

Some studies also reported the total leukocyte counts,sometimes without further subdividing them into classes.While decreased circulating leukocytes has been associatedwith stress (generally because of redistribution rather thandestruction of cells) (Dhabhar, 2002), there was no clearpattern with the number of leukocytes in captivity. 53% ofstudies (9 of 17) showed no change in total white blood cellscompared to free-living animals by the end of the captivityperiod; 23.5% (4 of 17) showed a decrease in circulatingleukocytes; and 23.5% (4 of 17) showed an increase (captivityduration 3 days to 1 year, see Table 4).

Importantly, neither total leukocyte numbers nor the N orH:L ratio provide a very strong indication of immune capac-ity. Some researchers have used more direct measurements ofimmune functionality. The bacterial killing assay is a way todetermine how effectively fresh whole blood can eliminatebacteria. This assay has the advantage of determining thereal effectiveness of the immune system against pathogens(Millet et al., 2007). In the cururu toad, whole blood was lesseffective at killing bacteria after 13 days of captivity (de Assiset al., 2015) and in two other toad species, killing capacitydecreased by 60 but not 30 days (Titon et al., 2017, 2018).Similarly, in red knots held in captivity for 1 year, whole bloodwas less effective at eliminating two Staphylococcus speciesthan in wild living birds (though there was no difference inEscherichia coli elimination) (Buehler et al., 2008). In con-trast, there was an increased proportion of E. coli killed after3 weeks of captivity in house sparrows (Love et al., 2017).

Another way to measure immune responsiveness is bymeasuring a proliferative response against non-specific anti-gens. In some studies, this is done by culturing a sample ofblood along with an antigen and quantifying cell division.In male brushtail possums, the proliferative response to theplant toxin phytohemagglutinin decreased over 20 weeks but

increased by 1 year (Baker et al., 1998). In female possums,the proliferative response increased from 11 to 15 weeks incaptivity, and then remained at that high level for at least ayear (Baker et al., 1998). In another study in male brushtailpossums, leukocyte proliferation to a Mycobacterium proteinderivative increased after 4 and 6 weeks of captivity, but onlywhen the animals were housed in high-density pens to createcrowding (Begg et al., 2004). The proliferative response tophytohemagglutinin can also be measured in-vivo if PHA isinjected into the skin and the degree of swelling is quantified.In zebra finches, there was no difference in the in vivo PHAresponse between newly captured birds and those held for 10or 16 days (Ewenson et al., 2001).

Two studies have attempted to quantify the strength of theadaptive immune system in captivity. In red knots, plasma wasplated with rabbit red blood cells. The degree of hemolysisand hemagglutination provided a measure of complementand natural antibody action. Hemolysis and hemagglutina-tion were similar in wild and captive birds when they weremeasured at the same time of year, which suggests that thestrength of the adaptive immune response is unaffected bycaptivity (Buehler et al., 2008). Conversely, newly capturedkillifish had a stronger response to antigen after immunizationthan 4–6-week captives, suggesting that the adaptive immunesystem was less effective after captivity (Miller and Tripp,1982).

Overall, there does not seem to be a single patternfor immune regulation with captivity. While captivity hasbeen shown to repress immune function in some species(e.g. reduced bacterial killing in red knots and toads), inother species, the immune system may be hyperactivated.For example, in house sparrows, gene expression for pro-inflammatory cytokines was elevated in captive birds(2- and 4-week captives) compared to newly caught animals,which was interpreted as hyperinflammation in captive birds(Martin et al., 2011). Changes in the immune responsewith chronic stress are thought to be most strongly tiedto GC release. However, the impacts of GCs on theimmune system can be complex. In the short term, GCstypically induce an immune response, while they can beimmunosuppressive over the long term, although theseinteractions tend to be context-dependent (Dhabhar andMcEwen, 1997; Martin, 2009). As the interaction betweenGCs and immunity is complex and context specific, and asthe interaction of GCs to captivity can be complex as well(see Changes in GCs during the adjustment to captivity), it isnot currently possible to predict whether captivity conditionswill result in appropriate or inappropriate immune activity.However, there has been limited work in this area.

Effects of captivity on the reproductivesystemCaptivity has well-documented negative impacts on reproduc-tive biology. In many species, captive breeding for research

..........................................................................................................................................................

21

Dow



ber 2022


Tabl

e4:

Chan

ges

inle

ukoc

ytes

durin

gca

ptiv

ity

Spec

ies

Stud

yde

sign

How

was

free

-livi

ngva

lue

esta

blis

hed?

Tim

efra

me

WBC

sH

orN

LH

orN

:Lra

tio

Cita

tion

Mam

mal

sSp

anis

hib

ex(C

apra

pyre

naic

ahi

span

ica)

Repe

ated

mea

sure

s;m

ultip

letim

epoi

nts

At-

capt

ure

sam

ple

14m

onth

s↓

–↓

↑(n.

c.)

(Pei

nado

etal

.,19

95)

Rhes

usm

acaq

ues

(Mac

aca

mul

atta

)Re

peat

edm

easu

res;

mul

tiple

timep

oint

sA

t-ca

ptur

esa

mpl

e1

year

↓↓

↑↓(

n.c.

)(L

illy

etal

.,19

99)

Brus

htai

led

poss

ums

(Tric

hosu

rus

vulp

ecul

a)

Repe

ated

mea

sure

s;m

ultip

letim

epoi

nts

Non

e—fir

stsa

mpl

eat

Wee

k1

ofca

ptiv

ity20

wee

ks–

–(B

aker

etal

.,19

98)

Belu

gaw

hale

(Del

phin

apte

rus

leuc

as)

Repe

ated

mea

sure

s;m

ultip

letim

epoi

nts

Atc

aptu

resa

mpl

ean

dfr

ee-li

ving

popu

latio

n

2.5

mon

ths

↑↑

↓↑(

n.c.

)(S

tAub

inan

dG

erac

i,19

89)

brus

htai

led

poss

ums

(Tric

hosu

rus

vulp

ecul

a)

Repe

ated

mea

sure

s;m

ultip

letim

epoi

nts

(diff

eren

thou

sing

cond

ition

s)

Non

e—un

clea

rw

hen

first

sam

ple

was

obta

ined

2m

onth

s–

––

–(n

.c.)

(Beg

get

al.,

2004

)

How

lerm

onke

y(A

loua

tta

cara

ya)

Repe

ated

mea

sure

s;pr

e-vs

post

-cap

tivity

At-

capt

ure

sam

ple

2m

onth

s–

––

–(n

.c.)

(San

chez

-Sar

mie

nto

etal

.,20

15)

Stel

lers

ealio

ns(E

umet

iopi

asju

batu

s)Re

peat

edm

easu

res;

pre-

vspo

st-c

aptiv

ityA

t-ca

ptur

esa

mpl

ean

dfr

ee-li

ving

popu

latio

n

2m

onth

s↓

(Mel

lish

etal

.,20

06)

Blac

krh

inoc

eros

(Dic

eros

bico

rnis

mic

hael

i)1

Repe

ated

mea

sure

s;pr

e-vs

post

-cap

tivity

Non

e–

first

sam

ple

afte

rstr

essf

ulca

ptur

e(u

pto

1ho

ur)

3–4

wee

ks↑

↓↑(

n.c.

)(K

ock

etal

.,19

99)

Vicu

ñas

(Vic

ugna

vicu

gna)

2Re

peat

edm

easu

res;

mul

tiple

timep

oint

sA

t-ca

ptur

esa

mpl

e312

days

––

––

(Bon

acic

and

Mac

dona

ld,

2003

)

Bird

sRe

dkn

ots

(Cal

idris

canu

tus)

Capt

ive

vsfr

ee-li

ving

popu

latio

nFr

ee-li

ving

popu

latio

n∼1

year

–↓

–↓(

n.c.

)(B

uehl

eret

al.,

2008

)

Ruff

(Phi

lom

achu

spu

gnax

)Re

peat

edm

easu

res;

mul

tiple

timep

oint

sN

one—

does

nots

ayw

hen

first

sam

ple

take

nre

lativ

eto

capt

ure

1ye

ar–

(Pie

rsm

aet

al.,

2000

)

(Con

tinue

d)

..........................................................................................................................................................

22

Dow



ber 2022


Tabl

e4:

Cont

inua

tion

Spec

ies

Stud

yde

sign

How

was

free

-livi

ngva

lue

esta

blis

hed?

Tim

efra

me

WBC

sH

orN

LH

orN

:Lra

tio

Cita

tion

Gre

enfin

ches

(Chl

oris

chlo

ris)

Capt

ive

vsfr

ee-li

ving

popu

latio

nFr

ee-li

ving

popu

latio

n2

mon

ths

––

↑↓

(Sep

pet

al.,

2010

)Ze

bra

finch

es(T

aeni

opyg

iagu

ttat

a)Ca

ptiv

evs

free

-livi

ngpo

pula

tion

Free

-livi

ngpo

pula

tion

10da

ys↓

↓(E

wen

son

etal

.,20

01)

2m

onth

s–

↓H

ouse

spar

row

(Pas

serd

omes

ticus

)4Re

peat

edm

easu

res;

early

-vs

late

-cap

tivity

Non

e—fir

stsa

mpl

e1–

2da

ysin

capt

ivity

1m

onth

––

↓↑(

n.c.

)(K

uhlm

anan

dM

artin

,201

0)

Her

ring

gull

(Lar

usar

gent

atus

)Re

peat

edm

easu

res;

mul

tiple

timep

oint

sA

t-ca

ptur

esa

mpl

e4

wee

ks↑

↑–

↑(n.

c.)

(Hoff

man

and

Leig

hton

,198

5)

Rufo

us-c

olla

red

spar

row

s(Z

onot

richi

aca

pens

is)

Capt

ive

vsfr

ee-li

ving

popu

latio

nFr

ee-li

ving

popu

latio

n2

wee

ks↑

↓↑

(Rui

zet

al.,

2002

)

Rept

iles

Gar

ters

nake

s(T

ham

noph

isel

egan

s)

Repe

ated

mea

sure

s;pr

e-vs

post

-cap

tivity

At-

capt

ure

sam

ple

and

free

-livi

ngpo

pula

tion

4m

onth

s↑

(Spa

rkm

anet

al.,

2014

)

Am

phib

ians

Curu

ruto

ad(R

hine

llaic

teric

a)Re

peat

edm

easu

res;

pre-

vspo

st-c

aptiv

ityA

t-ca

ptur

esa

mpl

e3

mon

ths

↑–

(de

Ass

iset

al.,

2015

)Fi

jian

grou

ndfr

og(P

laty

man

tisvi

tiana

)Re

peat

edm

easu

res;

mul

tiple

timep

oint

sA

t-ca

ptur

esa

mpl

e15

days

↑↓

↑(N

aray

anan

dH

ero,

2011

)25

days

––

–

Mol

esa

lam

ande

rs(A

mby

stom

ata

lpoi

deum

)

Repe

ated

mea

sure

s;pr

e-vs

post

-cap

tivity

At-

capt

ure

sam

ple

10da

ys–

↓↑

(Dav

isan

dM

aerz

,200

8)

Fish

Kutu

m(R

utilu

sfris

iiku

tum

)Ca

ptiv

evs

free

-livi

ngpo

pula

tion

Free

-livi

ngpo

pula

tion

3da

ys↑

↑↓

↑(n.

c.)

(Nik

ooet

al.,

2010

)

Tim

efra

me

refe

rsto

the

long

estd

urat

ion

ofca

ptiv

itym

easu

red.

WBC

=to

talw

hite

bloo

dce

lls;H

=he

tero

phils

;N=

neut

roph

ils;L

=ly

mph

ocyt

es;n

.c.=

notc

alcu

late

d(in

this

case

,aco

unto

rper

cent

age

ofhe

tero

phils

orne

utro

phils

and

lym

phoc

ytes

was

mea

sure

din

the

pape

r,bu

tHor

N:L

ratio

was

notd

irect

lyco

mpa

red.

Pres

ence

/dire

ctio

nof

chan

gein

the

rcty

pes)

;↑or

↓=hi

gher

orlo

wer

than

free

-livi

ng;–

=no

chan

gefr

omfr

ee-li

ving

.1

Patt

ern

only

seen

inrh

inos

tran

sloc

ated

from

high

tolo

w(n

othi

ghto

high

)ele

vatio

n.2

Tota

lWBC

san

dN

:Lra

tioal

soco

mpa

red

tofr

ee-li

ving

wild

popu

latio

nsof

asi

mila

rspe

cies

—th

ere

was

nodi

ffere

nce.

3Co

mpa

rison

tova

lues

colle

cted

inan

othe

rstu

dyan

dsp

ecie

s(ll

amas

and

alpa

cas)

.4

Circ

ulat

ing

leuk

ocyt

esan

dsk

in-in

filtr

atin

gle

ukoc

ytes

wer

em

easu

red.

See

text

fors

kin

leuk

ocyt

epa

tter

ns.

..........................................................................................................................................................

23

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ber 2022


or conservation purposes can be a challenge. Even the housesparrow, so commonly used as a model species, does notreadily breed in captivity (Lombardo and Thorpe, 2009). In74% of studies (17 of 23), the transition to captivity resultedin reduced reproductive capacity in wild species (Table 5).Note, however, that these papers do not cover an extensiveliterature on captive breeding, including in individuals whohave spent decades in captivity or were born in captivity,which is beyond the scope of this review. Here, we focusonly on those papers that studied reproductive capacity ofrecent captives (only within the first year) and that examineda mechanism for reduced reproduction. There was no obvioustaxonomic pattern for species that had reduced reproductiveability in captivity compared to those that had no documentedreproductive problems. Duration of captivity did not appearto be a factor either. In one study of water frogs, reproductionin both males and females were negatively impacted by only3 days of captivity (Zerani et al., 1991), while in jack mack-erel, reproduction was inhibited after a full year of adjustingto captivity (Imanaga et al., 2014).

Different researchers measured different variables forreproductive capacity. Many studies analyzed reproductivesteroid hormones (primarily testosterone in males andestrogen and/or progesterone in females). However, othervariables were also measured, including gonad size anddevelopment, behavior and gamete development. In housesparrows, Lombardo and Thorpe (2009) found decreasedsperm production, reduced testes size and a change in beakcolor from breeding-season black to wintering brown after3 months of captivity. Female anole lizards experienced arapid decrease in plasma vitellogenin (a protein necessaryfor yolk production) followed by regression of developingfollicles (Morales and Sanchez, 1996). In electric fish,behavioral differences between males and females werereduced in captivity until they disappeared or even reversed.This occurred concurrently with decreases in testosteroneand 11-ketotestosterone (a potent fish androgen) in males(Landsman, 1993).

The reduction of reproductive capacity might be tied toGC levels. GCs can be powerful suppressors of reproductivesteroids (Sapolsky et al., 2000). Prolonged GC exposure canlead to decreased production of testosterone or estradiol,which can then have downstream effects on gonad devel-opment, egg maturation, sperm production and behavior. Ingreen treefrogs, a decrease in sex steroids was concurrentwith an increase in GCs (Zerani et al., 1991). However, inblack rhinos, males had suppressed fecal testosterone andfemales had suppressed fecal progestins even though GClevels were below free-living levels for most of the captivityperiod (Linklater et al., 2010).

Captivity did not always result in suppression of repro-duction but in most studies that did not show an effectof captivity, reproductive hormones were the only variablesmeasured. The only exception was in the brown treesnake,where 3 days of captivity did not affect either testosterone

or ovarian development (both were very low in free-livingand captive animals) (Mathies et al., 2001). However, anotherstudy in brown treesnakes found underdeveloped testes inmales after 4–8 weeks of captivity (Aldridge and Arackal,2005). Captivity may affect sexual variables differently inmales and females. For example, in water frogs held incaptivity for 2 weeks, only males appeared to be negativelyaffected by captivity (Gobbetti and Zerani, 1996), which isopposite what is typically expected.

Overall, it appears that captivity tends to have a negativeimpact on reproduction in most species. However, there arerelatively few studies that specifically examine the repro-ductive physiology of newly-captured animals. Furthermore,given that many animals eventually do breed in captivitywhile others do not, it is not clear how long-lasting theseimpacts may be or why they impact some species more thanothers.

Adrenomedullary effects of captivityThe adrenomedullary arm of the stress response can be dif-ficult to measure. Measuring epinephrine or norepinephrinein the blood is relatively straightforward, but these hormonesincrease within seconds of disturbance, meaning that acquir-ing a free-living baseline in a wild animal is difficult with-out substantial acclimation to human presence. We excludedmost studies that measured epinephrine or norepinephrine,as sampling techniques between wild and captive animalsdiffered in ways that would obscure the meaning of theirresults. For example, plasma norepinephrine under anesthesia(collected within 50 minutes) decreased over 19 months ofcaptivity in rhesus macaques, though a free-living samplecould not be obtained under the same conditions (Lilly etal., 1999), and captive-raised bighorn sheep had a higherepinephrine response to a drop-net capture technique thandid free-living sheep, though they had similar norepinephrineresponses (Coburn et al., 2010).

Recording heart rate is another way to infer activity ofthe adrenomedullary system (Romero and Wingfield, 2016).Heart rate recordings typically involve the use of specializedand expensive equipment, but can give instantaneous updateson heart rate. In addition, scientists can measure heart ratevariability, which gives a metric of how much relative controlthe sympathetic and parasympathetic nervous systems haveover heart rate (Romero and Wingfield, 2016). However,depending on the type of heart rate recording device, it may beimpossible to obtain baseline free-living heart rates. Althoughseveral researchers have had success measuring heart ratein free-living animals (e.g. white-eyed vireos; Bisson et al.,2009), to our knowledge, there has not yet been a study thatdirectly compares heart rate in free-living and captive animalsof the same species.

Heart rate has been measured in only a few species duringthe transition to captivity. In newly-captured bighorn sheep,

..........................................................................................................................................................

24

Dow



ber 2022


Tabl

e5:

Repr

oduc

tive

effec

tsof

capt

ivity

inw

ildan

imal

s(if

mul

tiple

times

ofye

arw

ere

exam

ined

,onl

ybr

eedi

ngse

ason

isin

clud

edin

this

tabl

e)

Hor

mon

alch

ange

sdu

ring

adju

stm

entt

oca

ptiv

ity

Spec

ies

Stud

yde

sign

Tim

efra

me

Vari

able

mea

sure

dH

oww

ere

free

-livi

ngst

ate

esta

blis

hed?

Cita

tion

Repr

oduc

tive

capa

city

decr

ease

din

capt

ivity

Mam

mal

sW

hite

rhin

o(C

erat

othe

rium

sim

um)

Repe

ated

mea

sure

s;m

ultip

letim

epoi

nts

75da

ysFe

calT

(mal

es)a

ndPr

oges

tin(fe

mal

es)

At-

capt

ure

sam

ples

(Lin

klat

eret

al.,

2010

)

Blac

krh

ino

(Dic

eros

bico

rnis

)Re

peat

edm

easu

res;

mul

tiple

timep

oint

s60

days

Feca

lT(m

ales

)and

prog

estin

(fem

ales

)A

t-ca

ptur

esa

mpl

es(L

inkl

ater

etal

.,20

10)

Mou

sele

mur

(Mic

roce

busm

urin

us)

(♀onl

y)

Path

olog

yof

dead

capt

ive

anim

als

Varia

ble—

usua

llyye

ars

inca

ptiv

ityH

isto

logi

cal

exam

inat

ion

ofre

prod

uctiv

eor

gans

(folli

cula

rgro

wth

)

Repr

oduc

tive

path

olog

yin

crea

sed

with

capt

ivity

leng

th

(Per

ret,

1982

)

Bird

sBr

own-

head

edco

wbi

rd(M

olot

hrus

ater

)(♂o

nly)

1

Capt

ive

vsfr

ee-li

ving

popu

latio

n6

mon

ths+3

mon

ths

phot

ostim

ulat

ion

Gon

adsi

zean

dpl

asm

aT

Free

-livi

ngpo

pula

tion

(Duf

tyJr

and

Win

gfiel

d,19

86)

Hou

sesp

arro

w(P

asse

rdom

estic

us)

(♂)Re

peat

edm

easu

res;

mul

tiple

timep

oint

s3

mon

ths

Sper

mpr

oduc

tion,

beak

colo

r,te

stes

size

At-

capt

ure

sam

ples

and

free

-livi

ngpo

pula

tion

(Lom

bard

oan

dTh

orpe

,200

9)

Rept

iles

Brow

ntr

eesn

akes

(Boi

gairr

egul

aris

)(♂)

Capt

ive

vsfr

ee-li

ving

popu

latio

n4–

8w

eeks

Sexu

alm

atur

ity(t

este

sde

velo

pmen

t)Fr

ee-li

ving

popu

latio

n(A

ldrid

gean

dA

rack

al,2

005)

Ano

leliz

ard

(Ano

lispu

lche

llus)

(♀)M

ultip

letim

epoi

nts;

diffe

rent

indi

vidu

als

4w

eeks

Plas

ma

vite

lloge

nin;

ovar

yst

ate2

Free

-livi

ngpo

pula

tion

(Mor

ales

and

Sanc

hez,

1996

)

Tree

lizar

d(U

rosa

urus

orna

tus)

(♂)Re

peat

edm

easu

res;

mul

tiple

timep

oint

s3

wee

ksPl

asm

aT

At-

capt

ure

sam

ples

(Moo

reet

al.,

1991

)

Snap

ping

turt

le(C

hely

dra

serp

entin

a)Re

peat

edm

easu

res;

mul

tiple

timep

oint

s1

wee

kPl

asm

aT3

At-

capt

ure

sam

ple

(Mah

mou

det

al.,

1989

)

Am

phib

ians

Wat

erfr

og(R

ana

escu

lent

a)(♂)

Repe

ated

mea

sure

s;m

ultip

letim

epoi

nts

2w

eeks

Plas

ma

Tan

dE2

Atc

aptu

resa

mpl

es(G

obbe

ttia

ndZe

rani

,199

6)

Wat

erfr

og(R

ana

escu

lent

a)Re

peat

edm

easu

res;

mul

tiple

timep

oint

s3

days

Plas

ma

Tan

dE2

4A

tcap

ture

sam

ple

(Zer

anie

tal.,

1991

)

(Con

tinue

d)

..........................................................................................................................................................

25

Dow



ber 2022


Tabl

e5:

Cont

inua

tion

Hor

mon

alch

ange

sdu

ring

adju

stm

entt

oca

ptiv

ity

Spec

ies

Stud

yde

sign

Tim

efra

me

Vari

able

mea

sure

dH

oww

ere

free

-livi

ngst

ate

esta

blis

hed?

Cita

tion

Toad

(Rhi

nella

icte

rica)

Capt

ive

vsfr

ee-li

ving

popu

latio

n,m

ultip

letim

epoi

nts

1w

eek

Plas

ma

TFr

ee-li

ving

popu

latio

n(T

iton

etal

.,20

18)

Toad

(Rhi

nella

schn

eide

ri)Re

peat

edm

easu

res;

mul

tiple

timep

oint

s60

days

Plas

ma

TA

t-ca

ptur

esa

mpl

e(T

iton

etal

.,20

17)

Fish

Jack

mac

kere

l(T

rach

urnu

sja

boni

cus)

(♀)Ca

ptiv

evs

free

-livi

ngpo

pula

tion

1ye

arEg

gm

atur

ity,

repr

oduc

tive

stag

e,gn

rhge

neex

pres

sion

5

Free

-livi

ngpo

pula

tion

(Iman

aga

etal

.,20

14)

Elec

tric

fish

(Gna

thon

emus

pete

rsii)

Repe

ated

mea

sure

s;m

ultip

letim

epoi

nts

37da

ysSe

x-sp

ecifi

cbe

havi

ors,

plas

ma

Tan

d11

KT(m

ales

)

Atc

aptu

resa

mpl

es(L

ands

man

,19

93)

Sard

ine

(Sar

dina

pilc

ardu

s)Ca

ptiv

evs

free

-livi

ngpo

pula

tion

4w

eeks

Gon

ados

omat

icin

dex

Free

-livi

ngpo

pula

tion

(Mar

calo

etal

.,20

08)

Red

gurn

ard

(Che

lidon

icht

hys

kum

u)(♀)

Mul

tiple

timep

oint

s;di

ffere

ntin

divi

dual

sA

ND

repe

ated

mea

sure

s;m

ultip

letim

epoi

nts

4da

ysPl

asm

aT,

E2,e

ggde

velo

pmen

tFr

ee-li

ving

popu

latio

n(C

lear

wat

er,

1997

)

No

diffe

renc

ein

repr

oduc

tive

capa

city

inca

ptiv

ity

Mam

mal

sA

rmad

illos

(Das

ypus

nove

mci

nctu

s)(♂)

Repe

ated

mea

sure

s;m

ultip

letim

epoi

nts

Up

to3

year

sPl

asm

aT

Free

-livi

ngpo

pula

tion

(Cze

kala

etal

.,19

80)

Bird

sW

hite

-cro

wne

dsp

arro

ws

(Zon

otric

hia

leuc

ophr

ys)6

Repe

ated

mea

sure

s;m

ultip

letim

epoi

nts

Up

toda

y20

or33

Plas

ma

LH,p

lasm

aT

(mal

eson

ly)

At-

capt

ure

sam

ple

(Win

gfiel

det

al.,

1982

)

(Con

tinue

d)

..........................................................................................................................................................

26

Dow



ber 2022


Tabl

e5:

Cont

inua

tion

Hor

mon

alch

ange

sdu

ring

adju

stm

entt

oca

ptiv

ity

Spec

ies

Stud

yde

sign

Tim

efra

me

Vari

able

mea

sure

dH

oww

ere

free

-livi

ngst

ate

esta

blis

hed?

Cita

tion

Rept

iles

Strip

edpl

atea

uliz

ard

(Sce

lopo

rusv

irgal

tus)

(♀)Re

peat

edm

easu

res;

mul

tiple

timep

oint

sU

pto

3m

onth

sPl

asm

aP,

Tan

dE2

7Fr

eeliv

ing

popu

latio

n(W

eiss

etal

.,20

02)

Skin

k(E

gern

iaw

hitii

)(♂)

Repe

ated

mea

sure

s;m

ultip

letim

epoi

nts

4w

eeks

Plas

ma

TA

t-ca

ptur

esa

mpl

es(J

ones

and

Bell,

2004

)

Brow

ntr

eesn

ake

(Boi

gairr

egul

aris

)M

ultip

letim

epoi

nts;

diffe

rent

indi

vidu

als

3da

ysPl

asm

aT

and

ovar

ian

folli

cle

deve

lopm

ent

Free

-livi

ngpo

pula

tion

(Mat

hies

etal

.,20

01)

Am

phib

ians

Wat

erfr

og(R

ana

escu

lent

a)(♀)

Repe

ated

mea

sure

s;m

ultip

letim

epoi

nts

2w

eeks

Plas

ma

Tan

dE2

8A

tcap

ture

sam

ples

(Gob

bett

iand

Zera

ni,1

996)

1D

iffer

entp

hoto

sim

ulat

ion

and

soci

alst

imul

atio

nte

sted

—m

axim

alte

stic

ular

regr

owth

(long

days

+fe

mal

es)s

tillb

elow

wild

,tho

ugh

inth

atgr

oup,

Tw

asth

esa

me

asw

ild.

2Vi

tello

geni

nle

vels

reco

vere

dby

E2us

e.3

Tsp

ikes

durin

gth

efir

st24

–48

hour

sof

capt

ivity

,but

decr

ease

sbe

low

at-c

aptu

rele

vels

.4

E2sp

ikes

durin

gfir

stho

urs

ofca

ptiv

ity,b

utqu

ickl

yde

crea

ses

belo

wat

-cap

ture

leve

ls.

5E2

high

erin

capt

ive

than

wild

.6

Ther

ew

asa

tran

sito

ryin

crea

sein

LHat

arou

ndW

eeks

1–3

that

cam

eba

ckto

at-c

aptu

rele

vels

inm

ultip

leex

perim

ents

.7

Tlo

wer

inca

ptiv

ity,b

uton

lyaf

tere

gg-la

ying

.8

E2sp

ike

infir

st6

hour

sof

capt

ivity

butt

hen

retu

rns

toat

-cap

ture

leve

ls.

..........................................................................................................................................................

27

Dow



ber 2022


heart rate during restraint and blood sampling decreased fromDays 1–2 (when the animals were handled extensively andtransported) until Day 14 (Franzman, 1970). The heart rateof newly-captured European starlings was high compared tobirds held for more than a year in captivity but decreasedto the level of long-term captives within 24 hours (Dick-ens and Romero, 2009). The adrenomedullary response tocaptivity was slightly different in house sparrows. Daytimeheart rate was elevated above 1 month captive levels forat least 7 days post-capture (Fischer and Romero, 2016).These data led to a long-term repeated-measures investigationduring the first 6 weeks of captivity (Fischer et al., 2018).Heart rate tended to decrease until Day 18, then plateaued.Furthermore, there was a more profound effect on the heartrate response to a sudden noise in the starling study. Whilelong-term captives showed a robust increase in heart rateafter a loud noise, a typical adrenomedullary response, newly-captured birds had a virtually eliminated heart rate responsefor at least 10 days (Dickens and Romero, 2009). A reduc-tion in the startle response (as demonstrated in Europeanstarlings) could have negative consequences for animals thatare released from captivity into the wild (Dickens et al.,2009a). The adrenomedullary response to sudden noises orother startling events is an adaptation that allows animalsto survive sudden traumatic events, such as predator attacksor conspecific aggression. An impaired startle response couldresult in death if it persists after the animals are released fromcaptivity.

Overall, there are few studies examining the effects ofcaptivity on the adrenomedullary response. The patterns wesee in European starlings and house sparrows are different—itdoes not appear that there is a consistent heart rate responseto captivity in passerine birds, much less in all vertebrates.We believe this is an area ripe for future studies. As telemetryequipment becomes cheaper and more available, we hope tosee more investigations into the adrenomedullary response tocaptivity and other stressors.

Effects of captivity on seasonality ofhormone regulationSome studies examined seasonal differences in the response tocaptivity. Table 6 shows that the time of year when animalsare introduced to captivity can have a profound effect onhormonal changes. For example, baseline GCs might increasewhen free-living birds are in molt, decrease when free-livingbirds are breeding, and not change when free-living birds arecaptured during the winter or spring (Romero and Wing-field, 1999). Furthermore, Table 6 indicates that there is noconsistent pattern across seasons or taxonomic groups. Theimplications of these differences are currently unknown, butthe season of capture might partly explain the large variationacross studies summarized in Figs 2–4. Understanding whythere are seasonal differences in the acclimation to captivitywould be an important contribution to this field.

Other physiological consequences ofcaptivitySome studies, primarily in marine mammals, reported theeffects of captivity on thyroid hormone. Unfortunately, thereis not a consistent impact. For example, one study of belugawhales reported that thyroid hormone decreased over the firstfew days of captivity, but increased to a long-term stablelevel by day 11 (Orlov et al., 1991), whereas another studyreported that thyroid hormone decreased within the first fewdays and remained low throughout 10 weeks of captivity(St Aubin and Geraci, 1988). Similarly, rehabilitated harborseal juveniles held in captivity for 4 months had lower thyroidhormone than free-living juveniles (Trumble et al., 2013). Incontrast, long-term captive harbor porpoises had the samethyroid hormone levels as wild populations (Siebert et al.,2011) and in female brushtail possums, thyroid hormone waselevated from Weeks 6–13, the same period when the animalswere regaining weight they had lost in captivity (Baker et al.,1998). Clearly, more work is needed to determine the effectof captivity on thyroid hormone regulation.

Anatomical changes may also occur in captivity. Mountainchickadees showed remarkable reduction in hippocampalvolume after 4 months of captivity (LaDage et al., 2009), aneffect mimicked by black-capped chickadees after 4–6 weeksin captivity (Tarr et al., 2009). In neither species was thetelencephalon affected—the effect was localized to the partof the brain involved in location-based memory tasks. Thiseffect persisted even when the environment was enriched toinclude memory tasks (LaDage et al., 2009).

Captivity can lead to various pathologies. In a histo-logical study of mouse lemurs that died spontaneously incaptivity, lesions in the kidney were strongly correlated withcaptivity duration and with adrenal size (Perret, 1982). Theinvestigator also concluded that cardiac disease may resultfrom chronic adrenomedullary stimulation, although theydid not measure hormone concentrations directly (Perret,1982). Similarly, herring gulls developed amyloid deposits inthe blood vessels of their spleens after 28 days in captivity(Hoffman and Leighton, 1985). There may be many morehidden anatomical changes resulting from captivity, but fewstudies have looked for them.

Finally, recent data indicates that captivity can haveprofound effects at the DNA level. Bringing house sparrowsinto captivity resulted in an approximately doubling ofDNA damage in red blood cells (Gormally et al., 2019).The impact of this damage on the individual remains to bedetermined.

Amelioration of captivity stressCaptivity can cause a wide array of physiological changesin wild animals that are consistent with chronic stress andare likely to be detrimental to health. However, can anythingbe done to prevent these changes? Is there a way to protect

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Tabl

e6:

Seas

onal

effec

tsof

capt

ivity

Hor

mon

eSp

ecie

sH

oww

asfr

ee-li

ving

GCs

esta

blis

hed?

Capt

ivit

ydu

rati

onPr

e-br

eedi

ngBr

eedi

ngPo

st-

bree

ding

/m

olt

Win

ter

Cita

tion

Base

line

GCs

Mam

mal

sCa

nada

lynx

(Lyn

xca

nade

nsis

)fem

ales

Free

-livi

ngpo

pula

tion

Long

term

(unk

now

n)−

↑(F

anso

net

al.,

2012

)

Cana

daly

nx(L

ynx

cana

dens

is)m

ales

Free

-livi

ngpo

pula

tion

Long

term

(unk

now

n)↑

↑(F

anso

net

al.,

2012

)

Har

bors

eal(

Phoc

avi

tulin

a)Fr

ee-li

ving

popu

latio

nLo

ngte

rm(u

nkno

wn)

↓↓

↓(G

ardi

nera

ndH

all,

1997

)

Bird

sW

hite

-cro

wne

dsp

arro

w(Z

onot

richi

ale

ucop

hrys

gam

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)

Free

-livi

ngpo

pula

tion

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onth

sat

star

t−

↓↑

−(R

omer

oan

dW

ingfi

eld,

1999

)

Hou

sesp

arro

w(P

asse

rdo

mes

ticus

)Sa

me

indi

vidu

alpr

e-ca

ptur

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days

↑−

−−

(Lat

tinet

al.,

2012

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Rept

iles

Duv

auce

l’sge

coks

(Hop

loda

ctyl

usdu

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elli)

Free

-livi

ngpo

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tion

>1

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atth

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art

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arry

etal

.,20

10)

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ara

(Sph

enod

onpu

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rell

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94)

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ara

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phib

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-livi

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tion

2m

onth

sto

>1

year

↑↑

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erne

reta

l.,20

13)

Gre

enfr

og(R

ana

escu

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alpr

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Fish

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er(P

seud

ople

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)(ju

veni

le)

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ngpo

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tion

2m

onth

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t↓1

−(P

lant

eet

al.,

2003

)

(Con

tinue

d)

..........................................................................................................................................................

29

Dow



ber 2022


Tabl

e6:

Cont

inua

tion

Hor

mon

eSp

ecie

sH

oww

asfr

ee-li

ving

GCs

esta

blis

hed?

Capt

ivit

ydu

rati

onPr

e-br

eedi

ngBr

eedi

ngPo

st-

bree

ding

/mol

tW

inte

rCi

tati

on

Acut

est

ress

GCs

Bird

sW

hite

-cro

wne

dsp

arro

w(Z

onot

richi

ale

ucop

hrys

gam

belii

)

Free

-livi

ngpo

pula

tion

4m

onth

sat

star

t−

↓↑

−(R

omer

oan

dW

ingfi

eld,

1999

)

Hou

sesp

arro

w(P

asse

rdo

mes

ticus

)Sa

me

indi

vidu

alpr

e-ca

ptur

e5

days

−−

−↓

(Lat

tinet

al.,

2012

)

Am

phib

ians

East

ern

red-

spot

ted

new

t(N

otop

htha

lmus

virid

esce

ns)

Free

-livi

ngpo

pula

tion

>1

year

↑↑

−(B

erne

reta

l.,20

13)

Fish

Win

terfl

ound

er(P

seud

ople

uron

ecte

sam

eric

anus

)(ju

veni

le)

Free

-livi

ngpo

pula

tion

2m

onth

sat

star

t−

−(P

lant

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al.,

2003

)

TM

amm

als

Arm

adill

os(D

asyp

usno

vem

cinc

tus)

Free

-livi

ngpo

pula

tion

2w

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–3ye

ars

−−

−−

(Cze

kala

etal

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80)

Am

phib

ians

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enfr

og(R

ana

escu

lent

a)(♀)

Sam

ein

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dual

pre-

capt

ure

3da

ys↓

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(Zer

anie

tal.,

1991

)

Am

phib

ian:

gree

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og(R

ana

escu

lent

a)(♂)

Sam

ein

divi

dual

pre-

capt

ure

3da

ys↓

↓↓

(Zer

anie

tal.,

1991

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mph

ibia

nsA

mph

ibia

n:gr

een

frog

(Ran

aes

cule

nta)

(♀)Sa

me

indi

vidu

alpr

e-ca

ptur

e3

days

↓↓

↓(Z

eran

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l.,19

91)

Am

phib

ian:

gree

nfr

og(R

ana

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a)(♂)

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capt

ure

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anie

tal.,

1991

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ows

indi

cate

dire

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nof

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als

rela

tive

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hed

free

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ngle

vel.

Capt

ive

and

wild

mea

sure

men

tsw

ere

take

nat

the

sam

etim

eof

year

.GCs

gluc

ocor

ticoi

ds;T

test

oste

rone

;E2

estr

adio

l.1

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ayin

acqu

iring

wild

base

line.

..........................................................................................................................................................

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animals from the negative consequences of captivity stress?While this is not an exhaustive review of the solutionsthat have been tried, we offer some ideas that have beenattempted to relieve symptoms of chronic stress due tocaptivity conditions.

Adjusting the physical conditions of captivity may beone of the simplest ways to reduce symptoms of chronicstress. Transferal from outdoors cages to indoors cagesled to reduced reproductive hormones and behaviors inlong term captive European starlings (Dickens and Bentley,2014) and to weight loss and reduced immune functionin water voles (Moorhouse et al., 2007). Cage size anddensity are also important for the development of chronicstress. High density housing during the initial captivityperiod resulted in elevated GCs compared to low densityhousing in flounders (Nester Bolasina, 2011) and wedgesole (Herrera et al., 2016). However, reducing density bycaging animals individually can have negative consequences,particularly in social species. Housing brushtail possums ingroups eliminated the infection, weight loss and mortalitythat were seen when the animals were caged individually(McLeod et al., 1997). In male brown headed cowbirds,adding a female to the cage (previously solo housed) resultedin reduced plasma GCs, as well as increased testicularregrowth in photostimulated males (Dufty Jr and Wingfield,1986).

Many animals benefit from the use of behavioral enrich-ments to reduce abnormal behaviors that develop in captivity(reviewed in Mason et al., 2007). Enrichments have becomestandard practice in zoo environments and situations whereanimals are held long-term or bred in captivity. Enrichmentsconsist of providing animals with the means and motivationto practice a full range of natural behaviors, such as foragingopportunities, exercise opportunities and places to bathe ordust bathe. Even in temporary or laboratory conditions,environmental enrichments can be relatively easy to supply.However, we were unable to find any papers where the phys-iological benefits of enrichment techniques were specificallytested in newly captured animals. Using these techniques toaccelerate the adjustment to captivity would be an excitingavenue for future research.

Lighting conditions may be very important for visualspecies. European starlings show more behavioral signs ofchronic stress under fluorescent lights with a low flickerrate than a high flicker rate (Evans et al., 2012), but thelow flicker rate does not elicit a GC response (Greenwoodet al., 2004). Ultraviolet-deficient lighting resulted in higherbaseline GCs in European starlings, although immediatelyafter capture, this stressor may be too subtle to make adifference compared with the other stressors of captivity(Maddocks et al., 2002). Temperature conditions should alsobe carefully considered, particularly for poikilotherms. Warmconditions during the initial transfer to captivity resulted inhigh mortality in sardines (Marcalo et al., 2008) and higherGCs in cane toads (Narayan et al., 2012).

Overall, by matching captivity conditions as closely aspossible to conditions in the wild, with roomy cages, exposureto naturalistic lighting and temperature conditions and ani-mal densities kept relatively low, many animals will be betterable to adjust to captivity and may have reduced chronic stressas a result. However, naturalistic housing conditions may beimpractical for many situations. Furthermore, some stressorsassociated with captivity may be unavoidable. For example,nearly any visual or auditory contact with handlers resultedin a heart rate increase in two red-shouldered hawks (Pattonet al., 1985). Therefore, in some cases, it might be benefi-cial to use pharmaceuticals to reduce symptoms of chronicstress.

Tranquilizers or sedatives are perhaps the most obviousdrug classes to consider using in newly-captured animals.However, these may not be particularly effective at eliminat-ing chronic stress symptoms. A long-acting neuroleptic didnot result in many physiological changes in newly-caughtotters (Fernandez-Moran et al., 2004). Tranquilizers didnot impact any physiological variable in newly caughtimpala (Knox et al., 1990) or red-necked wallabies (Holzand Barnett, 1996), although they reduced behavioralagitation to human approach and handling in the laterstudy. Similarly, a long-acting tranquilizer changed behaviorbut not heart rate response to human approach in captivewildebeest (Laubscher et al., 2016). The anxiolytic andsedative diazepam did not affect GCs, heart rate, heartrate variability or activity in house sparrows during thefirst week of captivity (unpublished personal data). Overall,tranquilizers and sedatives do not appear to have long-termphysiological benefits in captive animals. However, theymay be useful in the short term. For example, by reducingphysical agitation, they may prevent animals from injuringthemselves during transport (e.g. in nurse sharks being movedinto captivity; Smith, 1992) or during necessary handlingby humans (e.g. in red-necked wallabies; Holz and Barnett,1996).

Another strategy for pharmaceutical reduction of symp-toms of chronic stress may be to chemically block the hor-mones of the stress response. The chemical agent mitotanecauses a reversible chemical adrenalectomy, which drasti-cally reduces circulating GCs (Sanderson, 2006). In housesparrows treated with mitotane immediately upon capture,baseline and stress induced GCs were drastically reducedduring the initial captivity period, but recovered to the level ofuntreated birds by Day 10 of captivity (Breuner et al., 2000).We investigated the effects of mitotane treatment during thefirst 7 days of captivity in house sparrows and found thatit reduced resting heart rate even when it did not causethe expected dramatic decrease in GC (unpublished personaldata). The adrenomedullary response can also be pharma-ceutically reduced by blocking the receptors of epinephrineand norepinephrine. We used alpha- and beta-blockers (whichinterfere with binding of epinephrine and norepinephrineto their receptors) during the first week to block chroniccaptivity stress in house sparrows. We found that while the

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beta-blocker propranolol had no effect on heart rate, it didprevent the increase in baseline GCs that we typically see innewly-captured members of this species (Fischer and Romero,2016).

The persistence of captivity effects afterreleaseThe physiological changes caused by captivity can persist evenafter animals have been released back into the wild. Chukarpartridges that were held in captivity 10 days and thenreleased to a new location than where they had originatedhad lasting changes to their GC regulation (decreased negativefeedback for at least 30 days, Dickens et al., 2009a). Redfoxes that were kept in captivity for 2 to 8 weeks were lesslikely to establish a stable territory upon release than foxesthat were caught and immediately released (Tolhurst et al.,2016). River otters kept in captivity for 10 months had lowersurvival than otters not kept in captivity (Ben-David et al.,2002). The captivity effect was strong enough that crude oilingestion (mimicking the state of oiled otters in rehabilitation)had no further effect on survival (Ben-David et al., 2002).Rehabilitated barn owls (Fajardo et al., 2000) and guillemots(Wernham et al., 1997) had much shorter life expectanciesthan wild birds.

However, captivity may not necessarily have lasting nega-tive impacts. In Grevy’s zebra, fecal GC metabolites were ele-vated in captivity, but decreased back to the wild norm quicklyafter release (Franceschini et al., 2008). Similarly, releasedEastern Bettongs decreased GC metabolites after release froma period of over 30 days of captivity (Batson et al., 2017).Hermann’s tortoises kept in captivity for 2–8 years followingan injury showed no difference in movement, thermoregula-tion or body condition compared to free-living animals afterrelease to the wild (Lepeigneul et al., 2014). Captivity up to3 months did not affect survival in Stellar’s sea lions (Shuertet al., 2015). Captivity may even have positive effects in somecases. For example, hedgehogs were more likely to survive atranslocation event if they were held in captivity for greaterthan 1 month compared to those held <6 days (Molony et al.,2006).

Whether an animal will be permanently negativelyimpacted by captivity or not may depend on the captivityconditions, species, time of year, method of release orindividual effects. Wild rabbits held for 2, 4, 6 or 8 weeks inquarantine before release did not differ in survival probability(Calvete et al., 2005). In another study in that species, GCsdid not change over the course of a quarantine period, butanimals with higher plasma and fecal GCs were more likely tosurvive, even though they had worse body condition (Cabezaset al., 2007). Saddlebacks were more likely to survive post-release when they had a robust GC response to a standardizedacute stressor (Adams et al., 2010). Therefore, captivity mayhave more profound effects on survival if it negatively andpermanently changes GC regulation.

ConclusionsCaptivity can cause weight loss, persistent changes in baselineand integrated GCs, changes in the immune system andreproductive suppression. These effects can last for monthsor years in some species, indicating that some species maynever truly adjust to captivity conditions. The welfare impli-cations of chronic captivity stress are obvious, and zoos andother institutions that hold animals in captivity long-termgenerally have strategies in place to minimize captivity stress.Breeding facilities (for conservation, research and agricul-ture/fisheries) are particularly invested in reducing chroniccaptivity stress, given its profound impact on the reproductivesystem. Figure 3 indicates that many species may continueto have elevated GCs months or years after capture, whileFigs 2 and 4 suggest that most animals will recover from theweight loss and elevated N or H:L ratios caused by the initialtransfer to captivity. Given that weight loss and changes toN or H:L ratio are affected by GCs, it is possible that with con-tinuing high GC concentrations, sensitivity to these hormonesdecreases in captive animals. The reproductive system tendsto be negatively impacted by captivity, presumably because ofelevated GC hormones. The negative effects of captivity arespecies-specific, some species adjust to captivity while othersdo not (see also Mason, 2010).

A captive animal may be physiologically quite differentthan a wild animal (Calisi and Bentley, 2009). Therefore,the confounding effects of captivity must be considered inphysiological studies using captive wild animals, even whenstress is not the focus of research. Animals that are held incaptivity for research might respond quite differently to arange of experimental treatments than a wild, free-living indi-vidual would. For example, environmental contaminants haddifferent effects on wild and captive sea otters (Levin et al.,2007), and experimentally induced chronic stress caused achange in fecal GCs in free-living but not captive Europeanstarlings (Cyr and Romero, 2008).

The existing literature indicates that the effects of captiv-ity on physiology are inconsistent. Some of the differencesbetween animals that adjust and do not adjust to captivitymight be explained by life-history features of the differentspecies (see Mason, 2010). For example, captive predatorsthat have large ranges in nature tend to show more behavioralanomalies and more infant mortality than those that naturallyhave smaller ranges (Clubb and Mason, 2003). However, itmay be possible to improve the physiological outcome fornewly-captured animals by adjusting the season of capture,improving and enriching housing, allowing for an appropri-ate adjustment period, and possibly by the careful use ofpharmaceuticals. Captivity stress will continue to be a factorin captive animal research, and the conditions, timing andduration of captivity must be considered as experiments aredesigned and interpreted.

Unfortunately, the results of this literature review do notsuggest useful overall and/or generalized guidelines to wildlife

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managers. The overall picture is that wild animals acclimateto captivity in a highly species-specific manner. However, themost important conclusion from this review is that collect-ing multiple measures of physiology, rather than restrictingstudies to a single measure (e.g. GC concentrations), willprovide a better picture of how well an individual or speciesis, or is not, coping with introduction to captivity.

FundingThis work was supported by the U.S. National Science Foun-dation [grant number IOS-1655269 to L.M.R.].

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Chronic captivity stress in wild animals is highly species-specific

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