This study compares breeding success and behavior of Humboldt penguins (Spheniscus humboldti) across multiple zoos to evaluate the influence of enclosure design and husbandry practices. Behavioral observations were conducted at Flamingo Land zoo over 8 months. Data on breeding success, behavior, enclosure features, and husbandry were also collected from questionnaires and literature. Breeding success was influenced by colony age and number of breeding pairs. Time spent swimming varied significantly between zoos and was used as an indicator of welfare. Regression models found swimming was best predicted by total enclosure area and land area per penguin. The results suggest optimal conditions for S. humboldti were not met and revised minimum standards for enclosure design are proposed

1. ForPeerReview
Husbandry and enclosure design influences on Humboldt
penguins
Journal: Zoo Biology
Manuscript ID ZOO-14-190.R1
Wiley - Manuscript type: Research Article
Date Submitted by the Author: 09-Jun-2016
Complete List of Authors: Marshall, Andrew; Centre for Integrated Research, Conservation and
Learning (CIRCLE), Environment Department, University of York; Flamingo
Land Resort
Deere, Nicolas; Centre for Integrated Research, Conservation and Learning
(CIRCLE), Environment Department, University of York; Flamingo Land
Resort; University of Kent, Durrell Institute of Conservation and Ecology
Little, Holly; Centre for Integrated Research, Conservation and Learning
(CIRCLE), Environment Department, University of York; Flamingo Land
Resort; University of Sheffield, Department of Animal and Plant Sciences
Snipp, Ross; Centre for Integrated Research, Conservation and Learning
(CIRCLE), Environment Department, University of York; Flamingo Land
Resort
Goulder, Jackie; Centre for Integrated Research, Conservation and
Learning (CIRCLE), Environment Department, University of York
Clarke, Stacey; Centre for Integrated Research, Conservation and Learning
(CIRCLE), Environment Department, University of York; Flamingo Land
Resort
Keywords: Exhibit design, Fecundity, GLM, Sphenisciformes, Welfare
John Wiley & Sons
Zoo Biology

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Title: Husbandry and enclosure design influences on Humboldt penguins
Short title: Humboldt penguin enclosure design
Authors: Marshall, A.R.1,2,
*, Deere, N.J. 1,2,3
*, Little, H.A.1,2,4
, Snipp, R.1,2
, Goulder, J. 1
, Mayer-
Clarke, S. 1,2
Addresses: 1
Centre for Integrated Research, Conservation and Learning (CIRCLE),
Environment Department, Wentworth Way, University of York, YO10 5NG, UK; 2
Flamingo
Land Ltd., Kirby Misperton, North Yorkshire, YO17 6UX, UK; 3
Durrell Institute of
Conservation and Ecology, School of Anthropology and Conservation, University of Kent,
Canterbury, Kent, CT2 7NR, UK; 4
Department of Animal and Plant Sciences, University of
Sheffield, S10 2TN, UK.
* These authors made equal contributions to this manuscript
Correspondence to: Andrew R. Marshall, CIRCLE, Environment Department, Wentworth Way,
University of York, YO10 5NG, UK. Email: andy.marshall@york.ac.uk.
Word count: 4,934
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Abstract: Multi-zoo comparisons of animal welfare are rare, and yet vital for ensuring
continued improvement of zoo enclosures and husbandry. Methods are not standardised for the
development of zoo enclosures based on multiple indicators, and case study species are
required. This study compares behaviour and breeding success to various enclosure and
husbandry parameters for the Humboldt penguin, Spheniscus humboldti, for the development of
improved enclosure design. Behavioural sampling was completed at Flamingo Land over a
period of eight months. Further data on behaviour, enclosure design and breeding success were
collected via questionnaires, visits to zoos, and literature review. Breeding success was
primarily influenced by colony age and number of breeding pairs, suggesting an important
social influence on reproduction. Across zoos, there was also significant variation in behaviour.
The proportion of time spent in water varied between zoos (2-23%) and was used as an indicator
of physical activity and natural behaviour. Regression models revealed that water-use was best
predicted by total enclosure area per penguin, followed by land area, with some evidence for
positive influence of pool surface area per penguin. Predominantly linear/curvilinear increases
in our biological indicators with enclosure parameters suggest that optimal conditions for
S. humboldti were not met among the selected zoos. We propose revised minimum conditions
for S. humboldti enclosure design, which exceed those in the existing husbandry guidelines. We
present a framework for the evaluation of zoo enclosures and suggest that a rigorous scientific
protocol be established for the design of new enclosures, based on multivariate methods.
Key words: exhibit design, fecundity, GLM, Sphenisciformes, swimming, welfare.
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Introduction1
The exhibition of captive animals to high welfare standards requires enclosures that promote2
species-typical behaviour (Fabregas et al., 2011), designed using an evidence-based framework3
(Dawkins, 2006; WAZA, 2005). Modern enclosure design is primarily determined using4
husbandry guidelines, which collate decades of practical experience. However, there is often5
little empirical evidence to support husbandry guidelines, raising concerns that some are driven6
by tradition rather than welfare (Hosey et al. 2013a). Furthermore, the “minimum standard”7
criteria adopted by husbandry guidelines can produce standardised enclosure designs,8
hampering further improvement (Melfi, 2009). The evaluation of zoo enclosures is also9
hindered by an absence of industry standard criteria to judge their success (Hancocks, 2010).10
Considering the multitude of variables that may influence animal welfare, the process of11
enclosure design would benefit from development of a rigorous scientific protocol for12
assessment and evaluation.13
14
Assessing zoo enclosures15
In terms of animal welfare, enclosure suitability can be assessed by the degree to which it meets16
the biological requirements of its inhabitants (Fabregas et al., 2011; WAZA, 2005). This17
requires consideration of the species’ natural habitat, ecology and behaviour, to ensure that their18
psychological and physiological needs are met (Hancocks, 2010; Kelling and Gaalema, 2011).19
Despite a trend towards exhibit naturalism, the dynamic complexity of the natural world has20
thus far proved challenging to replicate (Kawata, 2011). Zoos have often failed to maintain their21
inhabitants’ health, breeding status and wild behavioural repertoires, due to the restrictions22
imposed by a captive environment (Young, 2005) and limited scientific understanding of natural23
behaviour.24
Breeding success has been the most frequent indicator for measuring animal welfare in25
captivity, as previously implemented for a range of taxa (primates: Abello and Colell, 2006;26
carnivores: Clubb and Mason, 2007; birds: Farrell et al., 2000; invertebrates: Wisniewski,27
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2000). Failure to reproduce in captivity has been consistently linked to stress from sustained28
confinement in sub-optimal conditions (Descovich et al., 2012; Peng et al., 2007), and reduced29
opportunity for social interaction (Mallapur et al., 2006; Swaisgood and Schulte, 2010). Overall,30
if an enclosure does not provide an appropriate environment, the population will not have the31
physiological or behavioural capacity to breed, and the conservation objectives of the zoo will32
be compromised (Nicholas, 2007).33
Breeding success alone does not guarantee animal welfare (Dawkins, 1980; Swaisgood, 2007).34
Consequently, use of behavioural indicators of welfare has increased to determine psychological35
and physiological well-being (Hancocks, 2010; Kelling and Gaalema, 2011). Inadequate36
enclosures have been associated with behavioural abnormalities such as suppressed activity and37
stereotypies (Tarou et al., 2005). However, some species do not demonstrate overt behavioural38
responses to stress, and hence an absence of abnormalities does not necessarily indicate a39
suitable environment (Hill and Broom, 2009). Alternatively, activity budgets represent the40
standard metric in behavioural welfare assessment (Melfi and Feistner, 2002). Activity budgets41
are commonly employed in pairwise comparisons of enclosures, e.g. size (Mallapur and42
Chellam, 2002), complexity (Chang et al., 1999) and openness (Ross et al., 2010), with high43
activity levels assumed to indicate good physical health (Condon et al., 2003). However, simple44
pairwise approaches are vulnerable to single-site bias, and ignore the multiple features of animal45
husbandry that may influence behaviour. Hence, given uncertainty in the assessment of animal46
welfare using either behaviour or breeding information alone, we here adopt a dual-indicator47
approach. This approach is rare, for instance among 304 publications listed in all Thomson-48
Reuters Web of Science databases addressing enclosure design by WAZA-registered zoos49
between 1979-2013, only 26 considered multiple zoos, and only nine considered both behaviour50
and breeding together (of which only two employed multiple regression methods; Marshall,51
unpublished data).52
53
Humboldt penguin enclosure design54
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For statistically robust evaluation of zoo enclosures for welfare, species must be easy to55
observe, abundant in captivity, and must demonstrate sufficient variation between collections.56
The Humboldt penguin (Spheniscus humboldti) is one of the most common penguin species in57
captivity (Edgington, 1990), with a population of 2876 (919.897.306) in ISIS collections (ISIS,58
2013). Despite the abundance of S. humboldti, relatively little is known about the optimal59
features of enclosure design (AZA Penguin TAG, 2014).60
The only published study into S. humboldti enclosure design assessed the effects of enclosure61
parameters and demography on breeding success using questionnaire data (Blay and Cote,62
2001). Pool volume, concrete substrates and the number of breeding pairs had significant63
positive effects on breeding success. Use of chlorine has also been associated with increased64
mortality in S. humboldti (Blay and Cote, 2001), and stereotypic behaviour in other animals65
(Carlstead et al., 1999). However, improved knowledge of water balance with chlorine has led66
to reduced levels of stress in S. humboldti (de Voe, 2005).67
Penguin behaviour in relation to enclosure design has received even less attention than68
breeding. Swimming is a basic need in penguins and may represent an appropriate indicator for69
enclosure evaluation. A reluctance to swim is indicative of improper husbandry, poor physical70
health, and mental deterioration (Clarke, 2003).71
72
Aims and objectives73
Our aim is to use both breeding and behaviour to evaluate enclosure and husbandry influences74
on Spheniscus penguins, with primary focus on S. humboldti. We first determine measures of75
fecundity and behaviour of Spheniscus penguins from a range of zoos, through a combination of76
questionnaires, direct sampling and literature review. These measures are then statistically77
compared with features of enclosure design and husbandry. Using the results we evaluate the78
important design and husbandry features for S. humboldti welfare, and place emphasis on the79
importance of such a framework for future design of husbandry guidelines.80
81
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Materials/Methods82
Study site83
The principle study site comprised a population of 25 S. humboldti (10.10.5; two deaths and84
four births during sampling) at Flamingo Land (North Yorkshire, UK; 54˚12’19.8”N,85
0˚48’22.7”W; elevation 33m). The enclosure was approximately rectangular, with a land surface86
area of 196.8m². The concrete substrate included small areas of pebbles, a few shrubs, and a87
shallow stream (surface area 11.6m²) running into a pool (surface area 90.8m², volume88
118.0m³). There were two nesting areas with 17 nest boxes split between them, surrounded by89
walls and sparse vegetation. Flamingo Land was selected for study so that data could be used to90
design a new exhibit, later constructed in 2011.91
92
Breeding93
Following Blay and Cote (2001), breeding variables were calculated as the mean of three94
breeding seasons between 2007 and 2009. These variables included “egg productivity” (number95
of eggs laid female-1
year-1
), “hatching success” (the proportion of eggs that hatched) and “chick96
productivity” (the number of chicks that hatched and survived to reach sexual maturity pair-1
97
year-1
). These data were collected at the study site using a combination of taxon reports for98
years 2007-09 (S. Nasir, unpublished data) and personal communications with zoo staff.99
Additional data were collected from nine other UK zoos using a combination of questionnaires100
(n=7) and site visits (n=2). All participating collections were screened prior to data collection to101
ensure that they were not implementing measures to restrict breeding. These data were also102
combined with published data (Blay and Cote, 2001), following confirmation that methods used103
were equivalent (N. Blay, pers. comm.). For this comparison, our definitions of egg and chick104
productivity were adjusted for consistency with this earlier study, which followed a less-105
conventional definition of breeding success (egg/chicks per penguin, rather than per106
female/pair). In drawing this comparison we also acknowledge that unmeasured differences in107
zoo enclosure design spanning the 12 year period between studies could not be accounted for.108
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109
Behaviour110
Penguin behaviour was assessed at the study site over 112h across January-August 2009. This111
period spanned pre-nesting (26th
January–24th
February; n=27), nesting (eggs and chicks in nest;112
25th
February–25th
June; n=52) and post-nesting (chicks fledged and moult occurring; 26th
June–113
18th
August; n=33). These periods encompassed two biologically meaningful seasons to114
penguins, breeding (nesting) and moulting (post-nesting), while including a control period (pre-115
nesting) to help understand water-use in relation to the annual life-cycle. At the time of study116
the penguin enclosure was not accessible to visitors, in a quiet area of the zoo. Observation117
times were selected using a random number generator (Microsoft Excel “rand” function), from118
one or two nine 1h intervals (09:00–18:00) each day. Within each interval, six consecutive 5min119
scan samples were collected, recording the behaviour of all visible penguins. Data were then120
averaged across all six 5min intervals.121
An ethogram of behaviours (appendix 1) was developed from the literature (Merritt and King,122
1987; Welch, 1994), preliminary observations, and from discussion with zoo staff. Two123
observers collected the majority of data (SM and JG; 86h), with supplementary data from six124
additional zoo professionals (26h). To avoid inter-observer bias, methods were practiced in the125
presence of the principal investigator prior to data collection to establish consistency, and data126
were checked manually for obvious discrepancies in recording. Post-hoc inter-observer127
reliability tests identified no significant difference between observers both overall, and within128
each sampling period (Fleiss’s Kappa; Fleiss, 1971; n=6-8, κ=-0.02-0.01, p=0.35-0.67).129
Comparative behavioural data were extracted from pre-existing literature (n=5) from four130
European zoos (S. humboldti: Landau Zoo, Germany [Simeone et al., 2002], Dublin Zoo,131
Republic of Ireland [Devaney, 2009], and Newquay Zoo, UK [Harris, 2007]). For comparison,132
we also included data from the literature for the closely-related African penguin, S. demersus133
(Living Coasts, UK [data combined from two studies: Kidd, 2007; Nicholas, 2007]), which134
closely resembles S. humboldti in size, ecology, behaviour and overall appearance. In an effort135
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to increase practical use of student research (Rose et al., 2014), two of the behavioural studies136
used were undergraduate theses. Both theses were assessed for quality in accordance with the137
University of York’s Environment Department undergraduate dissertation marking scheme. To138
further ensure data quality, only basic behaviour classes were used, ethograms were assessed for139
similarity, and in the event of behavioural ambiguity, categories were merged. From each study,140
we calculated the proportion of time spent in water as an indicator of physical health.141
142
Predictor variables143
Husbandry and enclosure design parameters were measured to determine their influence on144
breeding success and water-use. These included number of penguins, colony age (number of145
years since the colony was first established at the collection), pool surface area (m2
), pool146
surface area per penguin (m2
penguin-1
), pool volume (m3
), pool volume per penguin (m3
147
penguin-1
), pool depth (m), land surface area (m2
), land surface area per penguin (m2
penguin-1
),148
“footprint” (i.e. total enclosure surface area per penguin = [land surface area + pool surface149
area]/number of penguins), water:land ratio, number of nest boxes per penguin, and whether150
chlorine was added to the water (presence/absence). These variables were selected for presumed151
influence on penguins from husbandry guidelines (Penguin TAG, 2005), previous literature152
(Blay and Cote, 2001), personal observations (JG), and personal communication with zoo staff.153
The only predictor variables available for comparison from the published literature were the154
number of breeding pairs and pool volume. We did not investigate nest box or enclosure floor155
substrate because of mixed surfaces, with complex variation across collections.156
157
Statistical analyses158
Statistical analyses were performed using R (v2.12.0; http://cran.r-project.org). All summary159
data were calculated as mean and 95% confidence intervals (95% CI; 10,000 bootstrapped160
samples). To avoid Type I errors, we employed the False Discovery Rate (FDR; Benjamini and161
Hochberg, 1995) correction of alpha values for repetitive testing.162
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163
(a) Influences on breeding and behaviour164
Generalised linear models (GLMs) were used to determine the relative influences on breeding165
and behaviour between the various predictor variables. In order to satisfy model assumptions, to166
reduce skew and improve linearity, Box Cox and square root (√) transformations were applied167
to relevant variables. To reduce the confounding effects of collinearity for modelling, predictor168
variables were then tested for intercorrelation using Pearson’s coefficient (r) and Variance169
Inflation Factors (VIF). Collinearity was considered serious if |r|≥0.7 and VIF≥5. Where two170
predictor variables were correlated, the one showing weakest correlation with the response171
variable was removed (Zuur et al., 2010).172
Multiple collinearity between predictor variables led us to employ two separate GLMs for each173
response variable, using alternative combinations of the least inter-correlated174
husbandry/enclosure parameters. GLMs were reduced using backward-forward stepwise175
selection using the Akaike Information Criterion (AIC) to produce a minimum adequate model.176
Full and stepwise reduced models were compared using analysis of deviance to ensure no177
significant reduction in explained deviance. Univariate GLMs were also performed for all178
variables not included in full models to verify that variables not included in multivariate models179
were not significantly related to breeding or behaviour. For all minimum adequate and180
univariate models we determined the probability that the slope estimate of each predictor181
variable was significantly different from zero (Quinn and Keough, 2002). Leverage was182
considered to be serious for Cook’s D≥1.0. Residual diagnostic plots were used to verify the183
absence of curvature and heteroscedasticity.184
For the GLM analyses, we used a Poisson error function to analyse chick productivity (because185
the data were counts), and a quasi-binomial error function for hatching success and for the186
proportion of time spent in water (because the data were proportions with over-dispersion;187
Crawley, 2005). For quasi-models we used quasi-AIC in preference to the AIC to compare188
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model fit (QAIC; Burnham and Anderson, 2002). For egg productivity, we used a negative189
binomial error function to deal with poor model diagnostics seen from Poisson alternatives,190
offset by the total number of females (equivalent to eggs female-1
year-1
; Zuur et al., 2009). For191
two models (colony age versus egg productivity; chlorine versus hatching success) we192
employed quadratic terms to test for apparent curvature.193
194
(b) Activity budget195
Activity budget data collected at the study site were compared to the other animal collections196
(n=4), using a G-test (Sokal and Rohlf, 1995). Only visible penguins could be assessed for their197
behavioural activity budgets, with those out of view allocated to an “out of sight” category. Low198
frequency (<1% of observation time) behavioural categories were combined (McDonald, 2014).199
For the proportion of time spent in water, G-tests were again employed to compare the study200
colony to the other sites. We also used G-tests to compare nesting, pre-nesting and post-nesting201
months to determine implications of seasonality on behaviour and future study design.202
203
Results204
Breeding205
The mean number of eggs laid was 26.7 eggs colony-1
year-1
(95% CI 10.1-46.7; n=10) and the206
mean number of chicks that hatched and survived to ≥1yr was 3.4 chicks colony-1
year-1
(1.2-207
5.9; n=10). From this, mean egg productivity was 0.92 eggs female-1
year-1
(0.41-1.52), mean208
chick productivity was 0.39 yearlings pair-1
year-1
(0.18-0.62) and mean hatching success was209
0.13 (0.07-0.19).210
211
Chick productivity did not produce a minimum adequate model and therefore a relationship212
could not be established with any husbandry/enclosure variables. Egg productivity was best213
modelled using number of breeding pairs and colony age, with water:land ratio near significant214
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(Table I; Fig. 1a–b). Hatching success had a significant positive relationship with water:land215
ratio and a near-significant negative relationship with chlorine (Table I; Fig. 1c).216
217
Table I: Husbandry/Enclosure Influences on Egg Productivity and Hatching Success218
GLM results for S. humboldti among 10 UK zoos, 2007-2009, including the direction of the219
trend (+/-), significance (P), percent deviance explained (%D) and model fit (AIC/QAIC). Bold220
type indicates significant variables at the 95% level (Egg productivity αFDR=0.0375; Hatching221
success: αFDR=0.025). Non-bold type indicates near-significant influences (0.05≤α<0.1).222
Minimum adequate models did not show reduced deviance from full models (Analysis of223
Deviance: p=0.06-0.82).224
Full models Minimum adequate models
Egg productivity (negative binomial)
(number of breeding pairs, colony age
[quadratic], pool depth, pool volume)
Egg productivity (negative binomial)
(nests pair-1
[Box Cox: λ=0.65],
water:land, chlorine, footprint)
Hatching Success (quasi-binomial)
(nests pair-1
[Box Cox: λ=0.65],
water:land, chlorine [quadratic],
footprint)
Pairs (+): P=0.0126, %D=19.9
Colony age [linear] (+): P=0.00441, %D=36.8
Colony age [quadratic] (-): P=0.00874, %D=28.6
[Colony age combined %D=39.4]
AIC=60.2, %D=63.1
Water:land (–): P=0.0517
AIC=63.7, %D=24.3
Water:land (+): P=0.0192, %D=44.1
Chlorine [linear] (-): P=0.0682, %D=22.2
QAIC=22.8, %D=76.1
225
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INSERT FIGURE 1 HERE226
227
Analysis of questionnaire data combined with data from the literature revealed a highly228
significant positive influence of √number of breeding pairs on both √chick productivity229
(P=0.003, %D=32.3, n=25) and √egg productivity (Fig. 2) and weak influence on √hatching230
success (P=0.075, %D=14.3, n=25). Logn pool volume was not found to influence hatching231
success (P=0.35, %D=5.8, n=17). Data for other husbandry/enclosure variables were not232
available for the published literature, nor data for pool volume versus chick or egg productivity.233
234
INSERT FIGURE 2 HERE235
236
Behaviour237
Significant variation was seen between activity budgets across all five zoos (Table II;238
69.1≤G≤119.4, P<0.001). The proportion of time spent in water also varied between zoos239
(23.6≤G≤45.0, P<0.001), with the exception of the present study versus Harris (G=2.4, P=0.12),240
Simeone et al. versus Kidd/Nicholas (G=1.5, P=0.22), Simeone et al. versus Devaney (G=0.1,241
P=0.70) and Kidd/Nicholas versus Devaney (G=0.8, P=0.36).242
243
Table II: Behavioural Activity Budget for five Spheniscus Penguin Colonies244
Data are expressed as mean percentage of time (and 95% CI where calculable).245
Behaviour This study Simeone et
al., 2002*
Devaney,
2009*
Harris,
2007*
Kidd/Nicholas,
2007*
Resting 18.9 (16.6–
21.3)
28.0 72.5 25.8 46.6
Preening 8.1 (7.2–9.2) 5.0 10.7 7.7 23.9
Terrestrial 2.3 (2.1–2.6) 5.7 3.4 10.5 9.1
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locomotion
Swimming 13.7 (12.1–
15.5)
2.0 2.5 23.3 4.2
Feeding 1.1 (1.0–1.3) 1.5 0.0 3.0 0.0
Interaction 1.2 (1.06–
1.35)
1.0 1.8 3.2 2.9
Out of
sight**
53.9
(47.5–60.9)
55.0 9.1 23.7 0.0
Other 0.9
(0.8–1.0)
1.8 0.0 2.8 13.2
Total water 17.0
(15.0–19.3)
2.0 2.5 23.3 4.2
Total land 83.0
(73.0–93.7)
98.0 97.5 76.7 95.8
Sample hours 112.0 40.5 13.3 19.0 42.5
Time of year
Species
Jan-Aug
S. humboldti
Jul, Dec
S. humboldti
Jan-Apr
S. humboldti
Feb-Apr
S. humboldti
Jul-Aug/Oct-
Nov
S. demersus
* Significant difference in activity budgets from this study (37.1≤G≤193.1, P<0.0001)246
** Out of sight penguins were typically resting in their nest boxes.247
248
The penguins demonstrated significant seasonal fluctuations in the proportion of time spent in249
water. A significantly greater proportion of time was spent in the water pre-nesting (42.3%)250
compared to nesting (9.1%; G=77.2, P<0.001) and post-nesting (6.4%; G=103.4, P<0.001).251
There was a small, non-significant decline in the proportion of time spent in water from the252
nesting to post-nesting period (2.7%; G=1.08, P=0.30).253
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254
The proportion of time spent in the water was best modelled using land surface area, and255
footprint (Fig. 1d-e), combined with near-significant predictor pool surface area penguin-1
256
(Table III). All remaining husbandry/enclosure parameters showed no relationship to time spent257
in water (p=0.47-0.98, QAIC=5.04-5.05).258
259
Table III: GLM Predictors of Proportion of Time Spent in Water by Five Zoo Penguin260
Colonies261
Included is the direction of the trend (+/-), significance (P), percent deviance explained (%D)262
and model fit (QAIC). Bold type indicates significant variables at the 95% level (αFDR=0.033).263
Non-bold type indicates near-significant variables (0.05≤α<0.1).264
Full models Minimum adequate model
Pool surface penguin-1
, Total
land surface area
Footprint, Pool volume [Box
Cox: λ=-0.38]
Total land surface area (+): P=0.0098, %D=82.4
Pool surface penguin-1
(+): P=0.085, %D=6.3
(QAIC = 68.637, %D = 98.8)*
Footprint (+): P = 0.0065
(QAIC = 196.4, %D = 92.5; Analysis of Deviance: p=0.054)
* No Analysis of Deviance because the minimum adequate model was the full model.265
266
Intercorrelation between predictors267
For the breeding analysis, intercorrelation was identified between the number of breeding pairs268
and the number of nest boxes (r=0.91), land surface area (r=0.83) and water:land ratio (r=-269
0.78). Six of the 12 enclosure variables (pool surface area, pool surface area penguin-1
, land270
surface area, land surface area penguin-1
, pool volume, pool volume penguin-1
) were also highly271
intercorrelated with one another in both the breeding (mean |r|=0.89) and behaviour (mean272
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|r|=0.93) analyses. For the behavioural analysis, pairs was highly intercorrelated with pool273
depth, pool volume, pool volume penguin-1
, water:land ratio and number of nest boxes (mean274
|r|=0.95).275
276
Discussion277
While our sample sizes are still modest and we advocate further research, our strongest278
statistical findings support modifications to S. humboldti enclosure design standards (Table IV),279
and our protocol has wider implications for enclosure evaluation (Fig. 3). These280
recommendations are important because the observed trends mostly do not reach a plateau281
(Figs. 1–2), suggesting that S. humboldti enclosures have not reached optimal design.282
283
Breeding284
Our observation that breeding success is most affected by group composition variables rather285
than enclosure parameters, supports previous work (Blay and Cote, 2001) and reflects the high286
degree of sociality expressed by S. humboldti (Duffy, 1983). The observed lack of relationship287
between enclosure parameters and chick productivity further suggests that the social welfare of288
the adults is the primary driver of breeding success, rather than the physiological health of289
young.290
Husbandry guidelines stress that penguins should be housed in colonies large enough to291
facilitate individual mate choice, and that small colonies may exhibit decreased reproductive292
output (AZA Penguin TAG, 2014). The observed rate of egg productivity increased linearly to293
9-10 breeding pairs in the two largest colonies. Colony size for wild S. humboldti is highly294
variable (Chile: 150–800 individuals; Hennicke and Culik, 2005), but they are only very rarely295
found in sub-colonies <20 adult birds when nesting (Boersma, 1991). Breeding success is296
highest in sub-colonies of 20–175 breeding pairs in wild Adelie penguins (Pygoscelis adeliae;297
Oelke, 1975), but increases with colony size in wild chinstrap penguins (Pygoscelis antarctica;298
Barbosa et al., 1997). However, the trade-off between top-down and bottom-up selection299
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pressures that drive wild colony size in Sphenisciformes (Ludynia et al., 2014) is absent in300
captive populations.301
The positive influence of social familiarity on reproductive success has been shown for a variety302
of taxa (Grabowska-Zhang et al., 2011; Martin and Shepherdson, 2012). Social bonds in birds303
reflect a lifetime of interactions for evaluating mate choice (Dubois et al., 1998), and for304
establishing relationships and parental behaviour (Fraser and Bugnyar, 2010). Accordingly, our305
best model of egg productivity included both the number of pairs and colony age (Table I).306
Therefore, breeding success in S. humboldti is reliant on well-established social bonds and307
presumably also long-term establishment of husbandry techniques. Observed low egg308
productivity among enclosures below 9 years old (Fig. 1b) suggests that zoos would benefit309
from adopting a breeding strategy of at least this timeframe (Table IV). However, potentially310
declining breeding success above 15 years suggests that our observation regarding enclosure311
size is most important for planning adequate space for ageing (and hence expanding) flocks.312
Among the husbandry measures, our results provide weak support for the previously observed313
influence of chlorinated water on breeding success (Blay and Cote, 2001). Improved knowledge314
regarding the safe use of chlorine in balance with other water properties (de Voe, 2005) may315
have now improved penguin welfare. Despite documented deleterious effects of chlorine, it is316
still recommended as a sterilising agent (AZA Penguin TAG, 2014). However, because of317
aforementioned ambiguity between studies, we do not give recommendations here on the use of318
chlorine.319
We are also reluctant to expand on husbandry guideline recommendations for water:land ratio320
of 1:2 (AZA Penguin TAG, 2014). The observed positive influence of water:land ratio on321
hatching success (Table I) may suggest that penguins require a sizeable area of land relative to322
pool size. This reflects the importance of security provided by increased land cover in species323
expressing a high degree of anthropogenic sensitivity (Ellenberg et al., 2006). Greater land324
cover also increases the distance between nest boxes and the water body, thus mitigating damp325
nest box conditions conducive to aspergillosis (Reavill, 1996). However, the positive326
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relationship for hatching success is confounded by our observed negative relationship between327
water:land ratio and egg productivity.328
Furthermore, while we could not verify a relationship between pool/enclosure size and breeding329
success, the observed high level of intercorrelation between predictor variables may have330
obscured findings and produced Type II errors. In particular, observed effects of land surface331
area, footprint, and pool surface area (the latter only near-significant) on swimming, and the332
effect of the number of pairs on breeding success, coupled with high intercorrelation between333
most variables associated with colony, pool and enclosure size, suggest that any increase in land334
or pool size is likely to result in improved penguin welfare.335
Quantitative comparison of breeding in captive animals to their wild counterparts may provide a336
further evaluation of zoo enclosures. For wild S. humboldti, breeding success data were only337
available for fledging, but not for egg/chick productivity or hatching success. In comparison to338
our observed mean chick productivity of 0.39 yearlings pair-1
year-1
(0.18-0.62), the fledging339
success of wild S. humboldti has ranged 0.13-1.51 fledglings pair-1
year-1
in Chile and Peru,340
depending on levels of disturbance (Ellenberg et al., 2006; Paredes et al., 2002). However,341
chicks fledge prior to one year of age (approximately 8 weeks old; pers. obs.), and hence are342
still prone to further mortality before they reach one year. Therefore further work is needed to343
determine whether limitations are imposed on breeding success by the captive environment.344
345
Behaviour346
Enclosure design has potential to increase activity levels of penguins. Primarily our data show347
the importance of space for physical health, through increased swimming seen with the area348
available per penguin (footprint), total land surface area, and pool surface area per penguin (the349
latter only near-significant). Our observed increase in water-use to a total enclosure area of350
21m2
per penguin, and a land surface area of 245–280m2
, suggests that husbandry guideline351
recommendations are insufficient for encouraging swimming (Table IV). Despite our observed352
lack of relationship between pool size and breeding success, a large pool may also encourage353
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development of reproductive behaviours in juveniles (Blay and Cote, 2001). Similarly,354
increased space has positively influenced activity in birds (Bennett et al. 2006; Mallapur et al.,355
2009), primates (Mallapur et al., 2005; Perkins, 1992) and also species-typical behaviour in356
carnivores (Aughtry, 1977; Brummer et al., 2010) and primates (Goerke et al., 1987;357
Nieuwenhuijsen and De Waal, 1982).358
While we have concluded that space is important for activity budgets, it is necessary to359
emphasise that enclosure complexity, rather than just size, must also be considered. Reductions360
in both size (Veasey et al., 1996) and complexity (Moreira et al., 2007) of the captive361
environment can restrict the diversity and flexibility of animal behaviour (Melfi and Feistner,362
2002). While peer-reviewed information is limited for zoo bird species, domestic chickens use363
more of their enclosure space when provided with perches (Rodriguez-Aurrekoetxea et al. 2014;364
Ventura et al. 2012). Although we consider additional variables to simply just total area, further365
studies would benefit from addressing measures of enclosure complexity, such as enrichment.366
Nevertheless, it is generally concluded that zoo enclosure size and complexity are equally367
important (Hosey et al. 2013a).368
While our statistical observations for behaviour are highly significant, they may have been369
influenced by the use of multiple independent studies, and warrant further investigation. Water-370
use can be subject to seasonal fluctuations, highlighting the importance of long-term data to371
mitigate temporal bias. Our observed reduction in water-use during breeding (nesting) and372
moulting (post-nesting) seasons shows similarity to wild S. humboldti (Luna-Jorquera et al.,373
2000; Luna-Jorquera and Culik, 2000). Both breeding and moulting require a level of374
dependency on energy reserves for survival (Guillemette et al., 2007) and hence reductions in375
both swimming and terrestrial locomotion are likely to be energy conservation strategies.376
However, there is inconsistency between the four other colonies (Table II), with the least and377
most active colonies both observed during the breeding season (swimming 2.5–23.3%; resting378
25.8–72.5%).379
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Water-use may also be related to feeding practices. Among the five behavioural studies, the380
colony with the highest level of swimming was mostly sampled around feeding times (23.3%381
swimming; Harris, 2007), whereas the most inactive colony was fed exclusively on land (72.5%382
resting; Devaney, 2009). Current husbandry guidelines recommend that penguins be fed by383
hand to ensure that each individual consumes a proportionate share of food, and to assist384
administering veterinary treatment (AZA Penguin TAG, 2014; Penguin TAG, 2005). However,385
the husbandry guidelines acknowledge that hand-feeding can lead to poor swimming and386
lethargy, and that “To encourage swimming, institutions may opt to pool feed”. Furthermore,387
wild penguins feed exclusively in water, and hence land-based feeding removes this opportunity388
to exhibit and develop a wild behaviour (Hui, 1988; Luna-Jorquera and Culik, 1999; Luna-389
Jorquera and Culik, 2000). To maximise physical activity, unrestricted access to water is a must,390
and we propose this should include feeding times, taking care to ensure approximately equal391
distribution of food. Accordingly, this minor husbandry alteration could provide an alternative392
strategy to improve penguin welfare where financial restrictions prevent pool enlargement.393
394
Table IV: Revised Enclosure Recommendations for Spheniscus Penguins395
Revisions are based on this study, compared with the current industry recommendations (AZA396
Penguin TAG, 2014). Recommendations based on behavioural observations are given in italics397
pending further investigation.398
Enclosure/husbandry variable Current Revised
Colony size 10 with approximately equal
sex ratio
≥9 pairs(1)
Colony age No recommendation ≥9 year strategy for
colony establishment(2)
Overall area per penguin (land +
water; m2
penguin-1
)
1.1 for first six penguins, then
0.6 per additional adult
≥21(3)
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Land surface area (m2
) 0.7 for first six penguins, then
0.4 per additional adult
≥245 total(4)
Feeding Hand-feed Feed in water(5)
(1)
Breeding success increased with the number of pairs, and was highest for the two colonies399
with 9–10 pairs (Fig. 1a).400
(2)
Colonies <9 years old had consistently low breeding success (Fig. 1b).401
(3)
Water-use increased with footprint, to the largest footprint of 21m2
penguin-1
(Fig. 1d).402
(4)
Water-use increased with land area, and was highest for the two enclosures with land area403
245-280m2
(Fig. 1e).404
(5)
Based on discussion regarding unrestricted access to water.405
406
Our observation of 2.5-23.0% time spent swimming suggests that captive S. humboldti swim407
less than their wild counterparts in Chile (conservative estimate 32.6%; Luna-Jorquera and408
Culik, 1999) and therefore presumably get less exercise. However, pressures that govern wild409
behaviour, such as competition, predation and foraging, are absent in captivity (Williams and410
Hoffman, 2009) and hence behavioural deviations may be a product of selection relaxation411
rather than enclosure design (Melfi, 2009). More specifically for S. humboldti, time spent at sea412
is influenced by environmental variables and anthropogenic influences that limit prey413
availability, visibility and therefore foraging effort (Culik, 2001; Culik and Luna-Jorquera,414
1997). Accordingly, where food is routinely provided in zoos without having to enter the water,415
a deviation from aquatic behaviour is expected, though not necessarily a welfare concern.416
417
Blueprint for Enclosure Evaluation and Design418
In the absence of industry standard criteria to appraise animal enclosures, we propose a419
framework for enclosure design (Fig. 3). The aim of this standardised framework is to420
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incorporate a rigorous, welfare-based evaluation, and to facilitate increased co-operation421
between animal collections, designers, senior zoo staff and research scientists.422
423
INSERT FIGURE 3 HERE424
425
Our blueprint begins with an evaluation of the enclosure. The varying influences on welfare and426
high levels of inter-correlation emphasise the complex nature of enclosure design. The cited427
literature and our own data emphasise the importance of considering multiple measures of428
enclosure design, husbandry and the five freedoms of animal welfare (reviewed by Hosey et al.429
2013b). Scientific input is therefore essential to facilitate multivariate analyses via cross-zoo430
comparison. The importance of forming academic links for improved scientific input to zoo431
management is well established (Benirschke, 1997; WAZA, 2005). While most zoos have at432
least one staff member with some level of research training, less than 10% have a dedicated433
research scientist (Marshall, unpublished data from British and Irish zoos). In the absence of434
zoo-based research staff, with adequate supervision and standardised methods, undergraduate435
research projects could be used to develop a behavioural database for captive species and hence436
facilitate cross-zoo comparisons.437
Further to the enclosure and husbandry considerations presented in our study, we also advocate438
assessment of visitor influence, e.g. variation in number, proximity to the animals, and noise439
levels, which could not be assessed in our off-show enclosure. Previous studies have440
documented the sensitivity of captive species to visitor number (Davey, 2007). However,441
despite S. humboldti showing a physiological sensitivity to anthropogenic disturbance in the442
wild (Ellenberg et al., 2006), similar evidence in captivity is lacking, yet desirable.443
The remaining steps of the blueprint are designed to encourage collaboration. While animal444
welfare should be the over-riding priority, involvement of a diverse range of expertise is likely445
to result in enclosures that benefit animals, staff and visitors. Finally, we emphasise the446
importance of re-evaluation for ensuring the long-term effectiveness of enclosures. Adaptive447
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management has become well-established as the guiding principle for conservation projects448
among the world’s major conservation NGOs (Conservation Measures Partnership, 2007).449
Adopting an adaptive management approach where biological indicators are monitored450
continually, would facilitate the evolution of management practices, animal welfare, and would451
generate baseline data that improve upon the predominance of time-limited studies.452
453
Conclusions454
1. S. humboldti breeding is primarily influenced by sociality among adults linked to colony size455
and age.456
2. S. humboldti water-use is mostly influenced by enclosure size, but obscured by sampling457
variation between studies.458
3. Regardless of confounding factors, land area and pool size are clearly important features for459
welfare, at least to accommodate increasing colony size.460
4. Increased sample sizes across seasons and zoos would further help to advance understanding.461
5. Establishment of a blueprint for enclosure design would help to integrate science and462
management for all captive animals.463
464
Acknowledgements465
Thanks to Birdland, Blackbrook Zoo, Dublin Zoo, Harewood Bird Gardens, Living Coasts,466
Marwell Wildlife, Paignton Zoo, Scarborough Sealife Centre, Sewerby Hall, South Lakes Zoo,467
Paradise Wildlife Park, Welsh Mountain Zoo, and Woburn Safari Park for completing468
questionnaires and/or supplying reports. Thanks to Flamingo Land staff, particularly Steve469
Nasir for advice and ISIS data, and to Linda Neil, Louise Naylor, Dean Cross and Martin Lees470
for behaviour data collection. Mayer received funding from the Aggregates Levy Sustainability471
Fund. Thanks to the BIAZA Research Committee for assistance with questionnaire472
development/approval.473
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Table legends
Table title: Table I: Husbandry/Enclosure Influences on Egg Productivity and Hatching
Success
GLM results for S. humboldti among 10 UK zoos, 2007-2009, including the direction of the
trend (+/-), significance (P), percent deviance explained (%D) and model fit (AIC/QAIC). Bold
type indicates significant variables at the 95% level (Egg productivity αFDR=0.0375; Hatching
success: αFDR=0.025). Non-bold type indicates near-significant influences (0.05≤α<0.1).
Minimum adequate models did not show reduced deviance from full models (Analysis of
Deviance: p=0.06-0.82).
Table title: Table II: Behavioural Activity Budget for five Spheniscus Penguin Colonies
Data are expressed as mean percentage of time (and 95% CI where calculable).
Table footnote:
* Significant difference in activity budgets from this study (37.1≤G≤193.1, P<0.0001)
** Out of sight penguins were typically resting in their nest boxes.
Table title: Table III: GLM Predictors of Proportion of Time Spent in Water by Five Zoo
Penguin Colonies
Included is the direction of the trend (+/-), significance (P), percent deviance explained (%D)
and model fit (QAIC). Bold type indicates significant variables at the 95% level (αFDR=0.033).
Non-bold type indicates near-significant variables (0.05≤α<0.1).
Table footnote: * No Analysis of Deviance because the minimum adequate model was the full
model.
Table title: Table IV: Revised Enclosure Recommendations for Spheniscus Penguins
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Revisions are based on this study, compared with the current industry recommendations (AZA
Penguin TAG, 2014). Recommendations based on behavioural observations are given in italics
pending further investigation.
Table footnote:
(1)
Breeding success increased with the number of pairs, and was highest for the two colonies
with 9–10 pairs (Fig. 1a).
(2)
Colonies <9 years old had consistently low breeding success (Fig. 1b).
(3)
Water-use increased with footprint, to the largest footprint of 21m2
penguin-1
(Fig. 1d).
(4)
Water-use increased with land area, and was highest for the two enclosures with land area
245-280m2
(Fig. 1e).
(5)
Based on discussion regarding unrestricted access to water.
Figure legends
Figure 1: Significant univariate GLM relationships, including egg productivity (average number
of eggs produced colony-1
year-1
) versus (a) number of breeding pairs and (b) colony age (years;
showing both linear and quadratic regression lines), (c) hatching success (the proportion of eggs
that hatched and survived ≥1yr) versus the ratio of water to land surface area, and proportion of
time spent in water versus (d) area per penguin (“footprint”; m2
penguin-1
), and (e) land surface
area (m2
).
Figure 2: GLM relationship between the number of breeding pairs versus (a) chick productivity
(chicks egg-1
year-1
; P=0.003, AIC=8.5, %D=32.3, and (b) egg productivity (eggs penguin-1
year-1
; P=0.0088, AIC=19.1, %D=26.3), using data from the present study (black dots) and the
published literature (white dots; Blay and Cote, 2001). Untransformed relationships are also
shown as insets to assist interpretation by animal managers.
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Figure 3: A blueprint for the design of new enclosures, as exemplified by S. humboldti in a
British zoo. This step by step process incorporates advice from Taxon Advisory Group (TAG)
chairs alongside enclosure evaluation, including comparisons across multiple animal
collections, to produce a simple in-house report (steps 1-3). This is circulated amongst any other
relevant colleagues for comment, preferably not restricting this to national boundaries (step 4).
These comments are integrated into the final report (step 5) which is circulated to internal staff
for comment (steps 6 and 7). This culminates in the construction of the new enclosure and
subsequent re-evaluation to ensure continued welfare over time (step 8).
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Appendix 1. Ethogram of behaviours used in the assessment of Spheniscus humboldti enclosure
suitability at Flamingo Land.
Water behaviours:
Float (head up) – birds move just their feet slowly or gently brush wings through water when
on belly. Head is held above water.
Float (head down) – as above, but head below water, probably scanning sideways.
Swim (surface) – the penguin swims actively on the water surface, with a clear bow wave.
Dive – penguin either dives in pool from side with no obvious sign of panic, or when in pool
swims underwater. This is just one category as diving into water is very brief in duration.
Porpoise – penguin jumps out of water like a dolphin.
Preen in water – roll onto side or back whilst at surface and preen/scratch. Sometimes roll in
water whilst jittering wings.
Play in water - juveniles porpoise in water like dolphins, tug at flippers and tails of other birds,
make mock attacks, and play with food in water by diving down and rushing up to floating food
as if hunting it.
Land behaviours:
Walk on land – waddling movement.
Run on land – fast waddling.
Grooming – preening can occur between pairs as a pair bonding behaviour. Individual birds
can also scratch themselves with beak and pull at feathers.
Shake dry – performed soon after leaving the water to dry feathers.
Aggressive – (1) bill to axilla: head is placed under the flipper and opposite flipper is raised.
May growl and lower flipper periodically, (2) sideways stare – penguin peers through narrowed
eye, (3) alternate stare – penguin stares from one eye then opposite eye, (4) pointing – bill is
pointed to individual who is annoying the pointer. Penguin leans towards other and may charge
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at other bird with beak agape, (5) locking of beaks – lock beaks and tug and grunt, (6) territorial
behaviour – vertical head movements in a figure of eight. Head is brought to feet and back up
whilst growling.
Mutual Display – pair facing each other and calling harshly and grunting. One may also shake
head.
Bowing – occurs between pairs at the nest, birds bow towards each other, often simultaneously.
Mutual trumpeting – occurs often between pairs, is when the pair both lean forward and then
upwards in synchrony, whilst trumpeting.
Trumpeting – juveniles may do this for attention.
Sexual – the “ecstatic” display is the most well-known, where a male pumps his chest and brays
to the sky, whilst arching the flippers backwards. May move head side-to-side when calling.
Mating can occur when the male stands behind female and beats his wings on her sides. He
may also rub underside of his head on her head and back. If she is receptive she will turn head
towards male and lift her tail, when the male can then mount.
Nesting – this can be recorded as a behaviour whenever a bird is in a nest box entrance or seen
going into a box. Also penguins gather twigs, stones, and grass.
Rest standing – the bird will be standing, not displaying any of the other behaviours mentioned,
but will have head up and/or looking around.
Rest lying – the bird is lying flat on belly with little movement, and not displaying any of the
other behaviours mentioned. May be asleep.
Play on land – juveniles tug at flippers and tails of other birds, make mock attacks and may
pick at novel objects.
Water or land based behaviours:
Feeding – eating or moving towards food. Prey attack behaviour is counted as feeding, where
the penguin circles its food in the water and then attacks it.
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Fear (anti-predator) – diving into water in response to predators or other potential threats.
Also gaping and braying when afraid on land.
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Figure 1: Significant univariate GLM relationships, including egg productivity (average number of eggs
produced colony-1
year-1
) versus (a) number of breeding pairs and (b) colony age (years; showing both
linear and quadratic regression lines), (c) hatching success (the proportion of eggs that hatched and
survived ≥1yr) versus the ratio of water to land surface area, and proportion of time spent in water versus
(d) area per penguin (“footprint”; m2
penguin-1
), and (e) land surface area (m2
).
138x138mm (96 x 96 DPI)
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Figure 1: Significant univariate GLM relationships, including egg productivity (average number of eggs
produced colony-1
year-1
) versus (a) number of breeding pairs and (b) colony age (years; showing both
linear and quadratic regression lines), (c) hatching success (the proportion of eggs that hatched and
survived ≥1yr) versus the ratio of water to land surface area, and proportion of time spent in water versus
(d) area per penguin (“footprint”; m2
penguin-1
), and (e) land surface area (m2
).
138x138mm (96 x 96 DPI)
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Figure 1: Significant univariate GLM relationships, including egg productivity (average number of eggs
produced colony-1
year-1
) versus (a) number of breeding pairs and (b) colony age (years; showing both
linear and quadratic regression lines), (c) hatching success (the proportion of eggs that hatched and
survived ≥1yr) versus the ratio of water to land surface area, and proportion of time spent in water versus
(d) area per penguin (“footprint”; m2
penguin-1
), and (e) land surface area (m2
).
138x138mm (96 x 96 DPI)
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Figure 1: Significant univariate GLM relationships, including egg productivity (average number of eggs
produced colony-1
year-1
) versus (a) number of breeding pairs and (b) colony age (years; showing both
linear and quadratic regression lines), (c) hatching success (the proportion of eggs that hatched and
survived ≥1yr) versus the ratio of water to land surface area, and proportion of time spent in water versus
(d) area per penguin (“footprint”; m2
penguin-1
), and (e) land surface area (m2
).
138x138mm (96 x 96 DPI)
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Figure 1: Significant univariate GLM relationships, including egg productivity (average number of eggs
produced colony-1
year-1
) versus (a) number of breeding pairs and (b) colony age (years; showing both
linear and quadratic regression lines), (c) hatching success (the proportion of eggs that hatched and
survived ≥1yr) versus the ratio of water to land surface area, and proportion of time spent in water versus
(d) area per penguin (“footprint”; m2
penguin-1
), and (e) land surface area (m2
).
138x138mm (96 x 96 DPI)
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Figure 2: GLM relationship between the number of breeding pairs versus (a) chick productivity (chicks egg-1
year-1
; P=0.003, AIC=8.5, %D=32.3), and (b) egg productivity (eggs penguin-1
year-1
; P=0.0088,
AIC=19.1, %D=26.3), using data from the present study (black dots) and the published literature (white
dots; Blay and Cote, 2001). Untransformed relationships are also shown as insets to assist interpretation by
animal managers.
138x138mm (96 x 96 DPI)
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Figure 2: GLM relationship between the number of breeding pairs versus (a) chick productivity (chicks egg-1
year-1
; P=0.003, AIC=8.5, %D=32.3), and (b) egg productivity (eggs penguin-1
year-1
; P=0.0088,
AIC=19.1, %D=26.3), using data from the present study (black dots) and the published literature (white
dots; Blay and Cote, 2001). Untransformed relationships are also shown as insets to assist interpretation by
animal managers.
138x138mm (96 x 96 DPI)
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Figure 3: A blueprint for the design of new enclosures, as exemplified by S. humboldti in a British zoo. This
step by step process incorporates advice from Taxon Advisory Group (TAG) chairs alongside enclosure
evaluation, including comparisons across multiple animal collections, to produce a simple in-house report
(steps 1-3). This is circulated amongst any other relevant colleagues for comment, preferably not restricting
this to national boundaries (step 4). These comments are integrated into the final report (step 5) which is
circulated to internal staff for comment (steps 6 and 7). This culminates in the construction of the new
enclosure and subsequent re-evaluation to ensure continued welfare over time (step 8).
190x275mm (96 x 96 DPI)
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