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Cited by 33Animal Behavior and Welfare StudiesAvian ecology and behaviorAnimal Behavior and Reproduction

Husbandry and enclosure influences on penguin behavior and conservation breeding

Marshall, Andrew R., Deere, Nicolas J., Little, Holly A., Snipp, Ross, Goulder, Jackie, Mayer-Clarke, Stacey·2016·Zoo Biology
DOI 10.1002/zoo.21313
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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 standardized for the development of zoo enclosures based on multiple indicators, and case study species are required. This study compares behavior and breeding success to various enclosure and husbandry parameters for the Humboldt penguin, Spheniscus humboldti, for the development of improved enclosure design. Behavioral sampling was completed at Flamingo Land over a period of 8 months. Further data on behavior, 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 behavior. The proportion of time spent in water varied between zoos (2-23%) and was used as an indicator of physical activity and natural behavior. 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. Zoo Biol. 35:385-397, 2016. © Wiley Periodicals, Inc.

AI snapshot

Written from the paper’s full text.

TL;DR

This study compares Humboldt penguin behavior and breeding success with enclosure and husbandry parameters across UK zoos to inform enclosure design. It finds breeding is mainly linked to colony age and number of breeding pairs, while water-use is mainly linked to enclosure space, and proposes revised minimum enclosure conditions exceeding existing guidelines.

Key findings

  • Breeding: egg productivity was best modelled by number of breeding pairs (+; P=0.0126, %D=19.9) and colony age (linear +; P=0.00441, %D=36.8; quadratic −; P=0.00874, %D=28.6); hatching success was positively related to water:land ratio (P=0.0192, %D=44.1) and near-significantly negatively related to chlorine (P=0.0682, %D=22.2); chick productivity produced no minimum adequate model.
  • Combined questionnaire and literature data: √number of breeding pairs positively influenced √chick productivity (P=0.003, %D=32.3, n=25) and √egg productivity, weakly influenced √hatching success (P=0.075, %D=14.3, n=25); log pool volume did not influence hatching success (P=0.35, %D=5.8, n=17).
  • Behavior: proportion of time in water varied 2–23% across zoos; at the study site total water was 17.0% (15.0–19.3) and swimming 13.7% (12.1–15.5). Water-use was best predicted by total land surface area (+; P=0.0098, %D=82.4), pool surface area penguin−1 (+; near-significant P=0.085, %D=6.3), and footprint (+; P=0.0065). Pre-nesting water use was 42.3% vs nesting 9.1% (G=77.2, P<0.001) and post-nesting 6.4% (G=103.4, P<0.001).
  • Revised recommendations: ≥9 breeding pairs, ≥9-year colony establishment strategy, ≥21 m² per penguin overall, ≥245 m² total land, and feeding in water.

Methods

  • Study site: 25 S. humboldti (10.10.5; two deaths and four births during sampling) at Flamingo Land; enclosure land 196.8 m², pool 90.8 m²/118.0 m³. Behavior was sampled over 112 h from January–August 2009 using 5-min scan samples across pre-nesting, nesting, and post-nesting periods; breeding variables were averaged over 2007–2009.
  • Additional breeding data came from nine other UK zoos via questionnaires (n=7) and site visits (n=2), plus published data; comparative behavior came from literature (n=5) from four European zoos, including S. demersus.
  • Analyses in R v2.12.0 used GLMs with Poisson, quasi-binomial, and negative binomial errors; AIC/QAIC stepwise selection; FDR correction; G-tests for activity budgets; transformations and collinearity checks.

Limitations

  • The paper states modest sample sizes and advocates further research; high intercorrelation among predictor variables may have obscured findings and produced Type II errors; behavioral comparison used multiple independent studies and warrants further investigation; water-use can fluctuate seasonally; unmeasured differences in zoo enclosure design over the 12-year gap between studies could not be accounted for; visitor influence could not be assessed in the off-show enclosure; nest box and substrate were not investigated because of mixed surfaces.
  • Evident from the text: the observational, correlational design across a small number of zoos (10 breeding, 5 behavior) cannot establish causation; inter-observer reliability kappa values were reported as −0.02–0.01 despite non-significant differences, indicating low agreement; two behavioral datasets were undergraduate theses, though they were quality-assessed.

Model-written summary. Check it against the paper before relying on it.

Integrity signals

Registry

Crossref · 10.1002/zoo.21313

Cites

75 of 75 references verified0 citation errors · 0 not checkable

Statistics

Nothing to recompute.

Claims the paper makes

12 of 88 cited sources checked · 4 supported · 0 flagged · accuracy not yet measured

  • Premisecitation
    § Introduction

    Breeding success has been the most frequent indicator for measuring animal welfare in captivity.

    “Breeding success has been the most frequent indicator for measuring animal welfare in captivity, as previously implemented for a range of taxa (primates: Abello and Colell, 2006; carnivores: Clubb and Mason, 2007; birds: Farrell et al., 2000; invertebrates: Wisniewski, 2000).”
    Quote in the paperNot a substantial claim1 of 3 sources checked
    • cites Abello and Colell, 2006 source
    • cites Clubb and Mason, 2007 source

      The Methods section uses infant mortality, a reproductive outcome, as one of two measures of captive carnivore welfare; the other is stereotypic behaviour. It does not say breeding success is the most frequent welfare indicator, and it describes conception rates as a possible measure rather than one used in this study. (LLM, conf=0.84)

      Experimental — accuracy not yet measured
    • cites Farrell et al., 2000 source
  • Interpretationcitation
    § Discussion

    The observed reduction in water-use during breeding and moulting seasons is similar to wild S. humboldti.

    “Our observed reduction in water-use during breeding (nesting) and moulting (post-nesting) seasons shows similarity to wild S. humboldti (Luna-Jorquera et al., 2000; Luna-Jorquera and Culik, 2000).”
    Quote in the paperNot a substantial claim1 of 2 sources checked
    • cites Luna-Jorquera et al., 2000

      Couldn’t be matched to a paper in Crossref, so it can’t be checked.

    • cites Luna-Jorquera and Culik, 2000 source

      The Food requirements during foraging and migration section discusses the energy and food needs of breeding Humboldt penguins, while Resting metabolic rate in water concerns energy expenditure in seawater (page numbers unavailable). Neither reports water-use reductions during breeding or moulting. Searches for seasonal water use, water intake, and moulting found no passage addressing the claimed comparison with wild birds. (LLM, conf=0.76)

      Experimental — accuracy not yet measured
  • Premisecitation
    § Discussion

    Wild penguins feed exclusively in water.

    “wild penguins feed exclusively in water, and hence land-based feeding removes this opportunity to exhibit and develop a wild behavior (Hui, 1988; Luna-Jorquera and Culik, 1999; Luna-Jorquera and Culik, 2000).”
    Quote in the paperSubstantial claim2 of 3 sources checked
    • cites Hui, 1988 source
    • cites Luna-Jorquera and Culik, 1999 source

      The Introduction and “Dive duration and foraging efficiency” section describe free-living Humboldt Penguins feeding on prey in coastal waters and foraging through dives (page numbers unavailable). They support aquatic foraging in this species, but do not establish that all wild penguins feed exclusively in water. (LLM, conf=0.84)

      Experimental — accuracy not yet measured
    • cites Luna-Jorquera and Culik, 2000 source

      The Introduction says Humboldt penguins travel from their breeding island to find food, and “Food requirements during foraging and migration” describes their foraging dives at sea. These passages support feeding in water for the Humboldt penguins studied, but do not establish that all wild penguins feed exclusively in water. (LLM, conf=0.86)

      Experimental — accuracy not yet measured
  • Interpretationown data
    § Discussion

    Breeding success is most affected by group composition variables rather than enclosure parameters.

    “Our observation that breeding success is most affected by group composition variables rather than enclosure parameters, supports previous work (Blay and Cote, 2001) and reflects the high degree of sociality expressed by S. humboldti (Duffy, 1983).”
    Quote in the paperSubstantial claim1 of 2 sources checked
    • cites Blay and Cote, 2001 source
    • cites Duffy, 1983 source
  • Premisecitation
    § Discussion

    Reductions in both size and complexity of the captive environment can restrict the diversity and flexibility of animal behavior.

    “Reductions in both size (Veasey et al., 1996) and complexity (Moreira et al., 2007) of the captive environment can restrict the diversity and flexibility of animal behavior (Melfi and Feistner, 2002).”
    Quote in the paperSubstantial claim2 of 3 sources checked
    • cites Veasey et al., 1996 source
    • cites Moreira et al., 2007 source
    • cites Melfi and Feistner, 2002 source

      The Discussion reports that macaques at one zoo moved and fed less than those at the others and identifies enclosure size and complexity as possible factors. It also says larger enclosures appeared associated with less resting, but complexity was not quantified. These passages support a possible effect on particular behaviours, not the broader claim that reduced size and complexity restrict behavioural diversity and flexibility in animals generally. (LLM, conf=0.84)

      Experimental — accuracy not yet measured
  • Classified as probably not a substantial claim. 35
  • May combine two claims. 41

  • Classified as probably not a substantial claim.

    Premisecitation
    § Introduction

    Activity budgets represent the standard metric in behavioral welfare assessment.

    “Alternatively, activity budgets represent the standard metric in behavioral welfare assessment (Melfi and Feistner, 2002).”
    Quote in the paperSubstantial claim1 of 1 sources checked
    • cites Melfi and Feistner, 2002 source

  • May combine two claims.

    Premisecitation
    § Discussion

    Social bonds in birds reflect a lifetime of interactions for evaluating mate choice, and for establishing relationships and parental behavior.

    “Social bonds in birds reflect a lifetime of interactions for evaluating mate choice (Dubois et al., 1998), and for establishing relationships and parental behavior (Fraser and Bugnyar, 2010).”
    Quote in the paperSubstantial claim1 of 2 sources checked
    • cites Dubois et al., 1998 source
    • cites Fraser and Bugnyar, 2010 source

      The Discussion (page unavailable) describes raven pair bonds as long-term investments tied to consistent interactions over time, supporting the relationship portion of the claim. Our copy does not link those bonds to parental behavior, and its findings concern primarily young, aviary-housed ravens rather than birds generally. The mate-choice clause is attributed to a different citation and is not assessed here. (LLM, conf=0.83)

      Experimental — accuracy not yet measured

  • May combine two claims.

    Premisecitation
    § Discussion

    Colony size for wild S. humboldti is highly variable (Chile: 150-800 individuals), but they are only very rarely found in sub-colonies <20 adult birds when nesting.

    “Colony size for wild S. humboldti is highly variable (Chile: 150–800 individuals; Hennicke and Culik, 2005), but they are only very rarely found in sub-colonies <20 adult birds when nesting (Boersma, 1991).”
    Quote in the paperNot a substantial claim1 of 2 sources checked
    • cites Hennicke and Culik, 2005 source
    • cites Boersma, 1991 source

  • Classified as probably not a substantial claim.

    Premisecitation
    § Discussion

    The positive influence of social familiarity on reproductive success has been shown for a variety of taxa.

    “The positive influence of social familiarity on reproductive success has been shown for a variety of taxa (Grabowska-Zhang et al., 2011; Martin and Shepherdson, 2012).”
    Quote in the paperSubstantial claim1 of 2 sources checked
    • cites Grabowska-Zhang et al., 2011 source

      The Abstract reports evidence suggesting that familiar neighbors improve reproductive outcomes in great tits. The Introduction also reports a positive finding for male red-winged blackbirds, but says direct evidence is limited and describes null findings in other birds. It does not establish a positive reproductive effect across a variety of taxa. (LLM, conf=0.88)

      Experimental — accuracy not yet measured
    • cites Martin and Shepherdson, 2012 source

  • May combine two claims.

    Interpretationown data
    § Discussion

    Captive S. humboldti swim less than their wild counterparts in Chile (conservative estimate 32.6%) and therefore presumably get less exercise.

    “Our observation of 2.5-23.0% time spent swimming suggests that captive S. humboldti swim less than their wild counterparts in Chile (conservative estimate 32.6%; Luna-Jorquera and Culik, 1999) and therefore presumably get less exercise.”
    Quote in the paperNot a substantial claim1 of 1 sources checked
    • cites Luna-Jorquera and Culik, 1999 source

      The At-sea activity section reports 301 hours of swimming and diving across 20 foraging trips by wild Humboldt penguins in northern Chile. It does not report the cited 32.6% estimate or specify the daily-time calculation needed to verify it. The captive comparison and presumed difference in exercise are the citing authors’ own inference, not a finding attributed to this source. (LLM, conf=0.82)

      Experimental — accuracy not yet measured

  • May combine two claims.

    Findingown data
    § Results

    Hatching success had a significant positive relationship with water:land ratio and a near-significant negative relationship with chlorine.

    “Hatching success had a significant positive relationship with water:land ratio and a near-significant negative relationship with chlorine (Table I; Fig. 1c).”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Findingown data
    § Results

    For the breeding analysis, intercorrelation was identified between the number of breeding pairs and the number of nest boxes, land surface area and water:land ratio.

    “For the breeding analysis, intercorrelation was identified between the number of breeding pairs and the number of nest boxes ( r =0.91), land surface area ( r =0.83) and water:land ratio ( r =-0.78).”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Findingown data
    § Discussion

    Our data show the importance of space for physical health, through increased swimming seen with the area available per penguin (footprint), total land surface area, and pool surface area per penguin (the latter only near-significant).

    “Primarily our data show the importance of space for physical health, through increased swimming seen with the area available per penguin (footprint), total land surface area, and pool surface area per penguin (the latter only near-significant).”
    Quote in the paperSubstantial claim
    • Rests on an assumption: Swimming is a basic need in penguins.

  • May combine two claims.

    Findingown data
    § Discussion

    There is inconsistency between the four other colonies in activity budgets, with the least and most active colonies both observed during the breeding season (swimming 2.5-23.3%; resting 25.8-72.5%).

    “However, there is inconsistency between the four other colonies (Table II), with the least and most active colonies both observed during the breeding season (swimming 2.5–23.3%; resting 25.8–72.5%).”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Findingown data
    § Results

    Egg productivity was best modelled using number of breeding pairs and colony age, with water:land ratio near significant.

    “Egg productivity was best modelled using number of breeding pairs and colony age, with water:land ratio near significant (Table I; Fig. 1a–b).”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Findingown data
    § Results

    Analysis of questionnaire data combined with data from the literature revealed a highly significant positive influence of √number of breeding pairs on both √chick productivity and √egg productivity.

    “Analysis of questionnaire data combined with data from the literature revealed a highly significant positive influence of √number of breeding pairs on both √chick productivity ( P =0.003, % D =32.3, n =25) and √egg productivity (Fig. 2) and weak influence on √hatching success ( P =0.075, %D =14.3, n =25).”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Findingown data
    § Results

    Chick productivity did not produce a minimum adequate model and therefore a relationship could not be established with any husbandry/enclosure variables.

    “Chick productivity did not produce a minimum adequate model and therefore a relationship could not be established with any husbandry/enclosure variables.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Findingown data
    § Discussion

    Water-use increased with land area, and was highest for the two enclosures with land area 245-280m2.

    “(4) Water-use increased with land area, and was highest for the two enclosures with land area 245-280m2 (Fig. 1e).”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Findingown data
    § Discussion

    Breeding success increased with the number of pairs, and was highest for the two colonies with 9-10 pairs.

    “(1) Breeding success increased with the number of pairs, and was highest for the two colonies with 9–10 pairs (Fig. 1a).”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Premisecitation
    § Introduction

    Some species do not demonstrate overt behavioral responses to stress, and hence an absence of abnormalities does not necessarily indicate a suitable environment.

    “However, some species do not demonstrate overt behavioral responses to stress, and hence an absence of abnormalities does not necessarily indicate a suitable environment (Hill and Broom, 2009).”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Hill and Broom, 2009 source

  • Classified as probably not a substantial claim. May combine two claims.

    Premisecitation
    § Introduction

    Activity budgets are commonly employed in pairwise comparisons of enclosures, with high activity levels assumed to indicate good physical health.

    “Activity budgets are commonly employed in pairwise comparisons of enclosures, e.g. size (Mallapur and Chellam, 2002), complexity (Chang et al., 1999) and openness (Ross et al., 2010), with high activity levels assumed to indicate good physical health (Condon et al., 2003).”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Condon et al., 2003

      Couldn’t be matched to a paper in Crossref, so it can’t be checked.

  • Classified as probably not a substantial claim.

    Premisecitation
    § Introduction

    Use of behavioral indicators of welfare has increased to determine psychological and physiological well-being.

    “Consequently, use of behavioral indicators of welfare has increased to determine psychological and physiological well-being (Hancocks, 2010; Kelling and Gaalema, 2011).”
    Quote in the paperSubstantial claim0 of 2 sources checked
    • cites Hancocks, 2010

      Couldn’t be matched to a paper in Crossref, so it can’t be checked.

    • cites Kelling and Gaalema, 2011 source

  • Probably not a substantial claim: may not pass S4 (based).

    Premisenone given
    § Abstract

    Multi-zoo comparisons of animal welfare are rare.

    “Multi-zoo comparisons of animal welfare are rare, and yet vital for ensuring continued improvement of zoo enclosures and husbandry.”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S2 (checkable).

    Premisecitation
    § Introduction

    Enclosure suitability can be assessed by the degree to which it meets the biological requirements of its inhabitants.

    “In terms of animal welfare, enclosure suitability can be assessed by the degree to which it meets the biological requirements of its inhabitants (Fabregas et al., 2011; WAZA, 2005).”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites Fabregas et al., 2011 source
    • cites WAZA, 2005

      Couldn’t be matched to a paper in Crossref, so it can’t be checked.

  • May combine two claims.

    Premisecitation
    § Introduction

    Failure to reproduce in captivity has been consistently linked to stress from sustained confinement in sub-optimal conditions and reduced opportunity for social interaction.

    “Failure to reproduce in captivity has been consistently linked to stress from sustained confinement in sub-optimal conditions (Descovich et al., 2012; Peng et al., 2007), and reduced opportunity for social interaction (Mallapur et al., 2006; Swaisgood and Schulte, 2010).”
    Quote in the paperSubstantial claim0 of 3 sources checked
    • cites Descovich et al., 2012 source
    • cites Peng et al., 2007 source
    • cites Mallapur et al., 2006 source

  • May combine two claims.

    Premisecitation
    § Introduction

    If an enclosure does not provide an appropriate environment, the population will not have the physiological or behavioral capacity to breed, and the conservation objectives of the zoo will be compromised.

    “Overall, if an enclosure does not provide an appropriate environment, the population will not have the physiological or behavioral capacity to breed, and the conservation objectives of the zoo will be compromised (Nicholas, 2007).”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Nicholas, 2007

      Couldn’t be matched to a paper in Crossref, so it can’t be checked.

  • Probably not a substantial claim: may not pass S2 (checkable).

    Premisecitation
    § Introduction

    Assessing enclosure suitability requires consideration of the species' natural habitat, ecology and behavior, to ensure psychological and physiological needs are met.

    “This requires consideration of the species' natural habitat, ecology and behavior, to ensure that their psychological and physiological needs are met (Hancocks, 2010; Kelling and Gaalema, 2011).”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites Hancocks, 2010

      Couldn’t be matched to a paper in Crossref, so it can’t be checked.

    • cites Kelling and Gaalema, 2011 source

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation
    § Introduction

    Despite a trend towards exhibit naturalism, the dynamic complexity of the natural world has thus far proved challenging to replicate.

    “Despite a trend towards exhibit naturalism, the dynamic complexity of the natural world has thus far proved challenging to replicate (Kawata, 2011).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Kawata, 2011 source

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation
    § Discussion

    Zoo enclosure size and complexity are equally important.

    “Nevertheless, it is generally concluded that zoo enclosure size and complexity are equally important (Hosey et al. 2013a).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Hosey et al. 2013a source

  • Classified as probably not a substantial claim.

    Study design and conductcitation
    § Introduction

    Data were combined with published data following confirmation that methods used were equivalent.

    “These data were also combined with published data (Blay and Cote, 2001), following confirmation that methods used were equivalent (N. Blay, pers. comm.).”
    Quote in the paperSubstantial claim0 of 2 sources checked
    • cites Blay and Cote, 2001 source
    • cites N. Blay, pers. comm.

      Couldn’t be matched to a paper in Crossref, so it can’t be checked.

  • Probably not a substantial claim: may not pass S2 (checkable). May combine two claims.

    Interpretationreasoning
    § Discussion

    Potentially declining breeding success above 15 years suggests that the observation regarding enclosure size is most important for planning adequate space for ageing (and hence expanding) flocks.

    “However, potentially declining breeding success above 15 years suggests that our observation regarding enclosure size is most important for planning adequate space for ageing (and hence expanding) flocks.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Premisecitation
    § Discussion

    Both breeding and moulting require a level of dependency on energy reserves for survival.

    “Both breeding and moulting require a level of dependency on energy reserves for survival (Guillemette et al., 2007)”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Guillemette et al., 2007 source

  • Classified as probably not a substantial claim.

    Premisecitation
    § Discussion

    Husbandry guidelines acknowledge that hand-feeding can lead to poor swimming and lethargy.

    “However, the husbandry guidelines acknowledge that hand-feeding can lead to poor swimming and lethargy, and that”
    Quote in the paperSubstantial claim0 of 2 sources checked
    • cites AZA Penguin TAG, 2014

      Couldn’t be matched to a paper in Crossref, so it can’t be checked.

    • cites Penguin TAG, 2005

      Couldn’t be matched to a paper in Crossref, so it can’t be checked.

  • May combine two claims.

    Premisenone given
    § Introduction

    Simple pairwise approaches are vulnerable to single-site bias, and ignore the multiple features of animal husbandry that may influence behavior.

    “However, simple pairwise approaches are vulnerable to single-site bias, and ignore the multiple features of animal husbandry that may influence behavior.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Interpretationown data
    § Discussion

    The observed trends mostly do not reach a plateau, suggesting that S. humboldti enclosures have not reached optimal design.

    “These recommendations are important because the observed trends mostly do not reach a plateau (Figs. 1–2), suggesting that S. humboldti enclosures have not reached optimal design.”
    Quote in the paperSubstantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Study design and conductnone given
    § Introduction

    Both undergraduate theses used were assessed for quality in accordance with the University of York's Environment Department undergraduate dissertation marking scheme.

    “Both theses were assessed for quality in accordance with the University of York's Environment Department undergraduate dissertation marking scheme.”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation
    § Introduction

    Use of chlorine has been associated with increased mortality in S. humboldti.

    “Use of chlorine has also been associated with increased mortality in S. humboldti (Blay and Cote, 2001), and stereotypic behavior in other animals (Carlstead et al., 1999).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Blay and Cote, 2001 source

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Study design and conductcitation
    § Introduction

    To avoid Type I errors, the False Discovery Rate correction of alpha values was employed for repetitive testing.

    “To avoid Type I errors, we employed the False Discovery Rate (FDR; Benjamini and Hochberg, 1995) correction of alpha values for repetitive testing.”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Benjamini and Hochberg, 1995 source

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation
    § Introduction

    Improved knowledge of water balance with chlorine has led to reduced levels of stress in S. humboldti.

    “However, improved knowledge of water balance with chlorine has led to reduced levels of stress in S. humboldti (de Voe, 2005).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites de Voe, 2005

      Couldn’t be matched to a paper in Crossref, so it can’t be checked.

  • Classified as probably not a substantial claim. May combine two claims.

    Premisecitation
    § Discussion

    Current husbandry guidelines recommend that penguins be fed by hand to ensure each individual consumes a proportionate share of food and to assist administering veterinary treatment.

    “Current husbandry guidelines recommend that penguins be fed by hand to ensure that each individual consumes a proportionate share of food, and to assist administering veterinary treatment (AZA Penguin TAG, 2014; Penguin TAG, 2005).”
    Quote in the paperSubstantial claim0 of 2 sources checked
    • cites AZA Penguin TAG, 2014

      Couldn’t be matched to a paper in Crossref, so it can’t be checked.

    • cites Penguin TAG, 2005

      Couldn’t be matched to a paper in Crossref, so it can’t be checked.

  • May combine two claims.

    Study design and conductown data
    § Discussion

    High intercorrelation between predictor variables may have obscured findings and produced Type II errors.

    “Furthermore, while we could not verify a relationship between pool/enclosure size and breeding success, the observed high level of intercorrelation between predictor variables may have obscured findings and produced Type II errors.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Premisecitation
    § Discussion

    Greater land cover increases the distance between nest boxes and the water body, thus mitigating damp nest box conditions conducive to aspergillosis.

    “Greater land cover also increases the distance between nest boxes and the water body, thus mitigating damp nest box conditions conducive to aspergillosis (Reavill, 1996).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Reavill, 1996

      Couldn’t be matched to a paper in Crossref, so it can’t be checked.

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation
    § Introduction

    Use of chlorine has been associated with stereotypic behavior in other animals.

    “Use of chlorine has also been associated with increased mortality in S. humboldti (Blay and Cote, 2001), and stereotypic behavior in other animals (Carlstead et al., 1999).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Carlstead et al., 1999 source

  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Study design and conductown data
    § Discussion

    The paper's statistical observations for behavior are highly significant but may have been influenced by the use of multiple independent studies.

    “While our statistical observations for behavior are highly significant, they may have been influenced by the use of multiple independent studies, and warrant further investigation.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Interpretationown data
    § Discussion

    The observed lack of relationship between enclosure parameters and chick productivity suggests that the social welfare of the adults is the primary driver of breeding success, rather than the physiological health of young.

    “The observed lack of relationship between enclosure parameters and chick productivity further suggests that the social welfare of the adults is the primary driver of breeding success, rather than the physiological health of young.”
    Quote in the paperSubstantial claim

  • Probably not a substantial claim: may not pass S2 (checkable).

    Interpretationown data
    § Discussion

    Observed low egg productivity among enclosures below 9 years old suggests that zoos would benefit from adopting a breeding strategy of at least this timeframe.

    “Observed low egg productivity among enclosures below 9 years old (Fig. 1b) suggests that zoos would benefit from adopting a breeding strategy of at least this timeframe (Table IV).”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Study design and conductown data
    § Introduction

    Post-hoc inter-observer reliability tests identified no significant difference between observers both overall, and within each sampling period.

    “Post-hoc inter-observer reliability tests identified no significant difference between observers both overall, and within each sampling period (Fleiss's Kappa; Fleiss, 1971; n=6-8, κ=-0.02-0.01, p=0.35-0.67).”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Fleiss, 1971 source

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Study design and conductnone given
    § Introduction

    Observation times were selected using a random number generator.

    “Observation times were selected using a random number generator (Microsoft Excel “rand” function), from one or two nine 1h intervals (09:00–18:00) each day.”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Premisecitation
    § Discussion

    Husbandry guidelines stress that penguins should be housed in colonies large enough to facilitate individual mate choice and that small colonies may exhibit decreased reproductive output.

    “Husbandry guidelines stress that penguins should be housed in colonies large enough to facilitate individual mate choice and that small colonies may exhibit decreased reproductive output (AZA Penguin TAG, 2014).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites AZA Penguin TAG, 2014

      Couldn’t be matched to a paper in Crossref, so it can’t be checked.

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Interpretationcitation
    § Discussion

    Improved knowledge regarding the safe use of chlorine in balance with other water properties may have now improved penguin welfare.

    “Improved knowledge regarding the safe use of chlorine in balance with other water properties (de Voe, 2005) may have now improved penguin welfare.”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites de Voe, 2005

      Couldn’t be matched to a paper in Crossref, so it can’t be checked.

  • May combine two claims.

    Premisecitation
    § Introduction

    A reluctance to swim is indicative of improper husbandry, poor physical health, and mental deterioration.

    “A reluctance to swim is indicative of improper husbandry, poor physical health, and mental deterioration (Clarke, 2003).”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Clarke, 2003 source

  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Premisecitation
    § Discussion

    Increased space has positively influenced activity in birds, primates and species-typical behavior in carnivores and primates.

    “Similarly, increased space has positively influenced activity in birds (Bennett et al. 2006; Mallapur et al., 2009), primates (Mallapur et al., 2005; Perkins, 1992) and also species-typical behavior in carnivores (Aughtry, 1977; Brummer et al., 2010) and primates (Goerke et al., 1987; Nieuwenhuijsen and De Waal, 1982).”
    Quote in the paperNot a substantial claim0 of 3 sources checked
    • cites Bennett et al. 2006 source
    • cites Mallapur et al., 2009 source
    • cites Mallapur et al., 2005 source

  • May combine two claims.

    Premiseown data
    § Discussion

    Chicks fledge prior to one year of age (approximately 8 weeks old) and hence are still prone to further mortality before they reach one year.

    “However, chicks fledge prior to one year of age (approximately 8 weeks old; pers. obs.), and hence are still prone to further mortality before they reach one year.”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites pers. obs.

      Couldn’t be matched to a paper in Crossref, so it can’t be checked.

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Study design and conductnone given
    § Introduction

    Unmeasured differences in zoo enclosure design spanning the 12 year period between studies could not be accounted for.

    “In drawing this comparison we also acknowledge that unmeasured differences in zoo enclosure design spanning the 12 year period between studies could not be accounted for.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Interpretationreasoning
    § Discussion

    Breeding success in S. humboldti is reliant on well-established social bonds and presumably also long-term establishment of husbandry techniques.

    “Therefore, breeding success in S. humboldti is reliant on well-established social bonds and presumably also long-term establishment of husbandry techniques.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Interpretationown data
    § Discussion

    The strongest statistical findings support modifications to S. humboldti enclosure design standards, and the protocol has wider implications for enclosure evaluation.

    “While our sample sizes are still modest and we advocate further research, our strongest statistical findings support modifications to S. humboldti enclosure design standards (Table IV), and our protocol has wider implications for enclosure evaluation (Fig. 3).”
    Quote in the paperSubstantial claim

  • Classified as probably not a substantial claim. May combine two claims.

    Study design and conductnone given
    § Introduction

    To avoid inter-observer bias, methods were practiced in the presence of the principal investigator prior to data collection to establish consistency, and data were checked manually for obvious discrepancies in recording.

    “To avoid inter-observer bias, methods were practiced in the presence of the principal investigator prior to data collection to establish consistency, and data were checked manually for obvious discrepancies in recording.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Premisecitation
    § Discussion

    Breeding success is highest in sub-colonies of 20-175 breeding pairs in wild Adelie penguins, but increases with colony size in wild chinstrap penguins.

    “Breeding success is highest in sub-colonies of 20–175 breeding pairs in wild Adelie penguins ( Pygoscelis adeliae ; Oelke, 1975), but increases with colony size in wild chinstrap penguins ( Pygoscelis antarctica ; Barbosa et al., 1997).”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites Oelke, 1975 source
    • cites Barbosa et al., 1997 source

  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Interpretationcitation
    § Discussion

    Despite the observed lack of relationship between pool size and breeding success, a large pool may also encourage development of reproductive behaviors in juveniles.

    “Despite our observed lack of relationship between pool size and breeding success, a large pool may also encourage development of reproductive behaviors in juveniles (Blay and Cote, 2001).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Blay and Cote, 2001 source

  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Premisecitation
    § Introduction

    Pool volume, concrete substrates and number of breeding pairs had significant positive effects on breeding success.

    “Pool volume, concrete substrates and the number of breeding pairs had significant positive effects on breeding success.”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Blay and Cote, 2001 source

  • Classified as probably not a substantial claim.

    Study design and conductnone given
    § Introduction

    All participating collections were screened prior to data collection to ensure that they were not implementing measures to restrict breeding.

    “All participating collections were screened prior to data collection to ensure that they were not implementing measures to restrict breeding.”
    Quote in the paperSubstantial claim

  • Classified as probably not a substantial claim. May combine two claims.

    Study design and conductreasoning
    § Introduction

    To further ensure data quality, only basic behavior classes were used, ethograms were assessed for similarity, and in the event of behavioral ambiguity, categories were merged.

    “To further ensure data quality, only basic behavior classes were used, ethograms were assessed for similarity, and in the event of behavioral ambiguity, categories were merged.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Interpretationown data
    § Conclusions

    S. humboldti water-use is mostly influenced by enclosure size, but obscured by sampling variation between studies.

    “2. S. humboldti water-use is mostly influenced by enclosure size, but obscured by sampling variation between studies.”
    Quote in the paperSubstantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation
    § Discussion

    Previous studies have documented the sensitivity of captive species to visitor number.

    “Previous studies have documented the sensitivity of captive species to visitor number (Davey, 2007).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Davey, 2007 source

  • May combine two claims.

    Interpretationcitation
    § Discussion

    Behavioral deviations may be a product of selection relaxation rather than enclosure design.

    “and hence behavioral deviations may be a product of selection relaxation rather than enclosure design (Melfi, 2009).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Melfi, 2009 source

  • Classified as probably not a substantial claim.

    Interpretationown data
    § Discussion

    The cited literature and the paper's own data emphasise the importance of considering multiple measures of enclosure design, husbandry and the five freedoms of animal welfare.

    “The cited literature and our own data emphasise the importance of considering multiple measures of enclosure design, husbandry and the five freedoms of animal welfare (reviewed by Hosey et al. 2013b).”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Hosey et al. 2013b source

  • May combine two claims.

    Interpretationreasoning
    § Discussion

    Where food is routinely provided in zoos without having to enter the water, a deviation from aquatic behavior is expected, though not necessarily a welfare concern.

    “Accordingly, where food is routinely provided in zoos without having to enter the water, a deviation from aquatic behavior is expected, though not necessarily a welfare concern.”
    Quote in the paperSubstantial claim
    • Rests on an assumption: Food is routinely provided in zoos without requiring penguins to enter the water.

  • May combine two claims.

    Premisecitation
    § Discussion

    While most zoos have at least one staff member with some level of research training, less than 10% have a dedicated research scientist.

    “While most zoos have at least one staff member with some level of research training, less than 10% have a dedicated research scientist (Marshall, unpublished data from British and Irish zoos).”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Marshall, unpublished data from British and Irish zoos

      Couldn’t be matched to a paper in Crossref, so it can’t be checked.

  • Probably not a substantial claim: may not pass S2 (checkable).

    Interpretationnone given
    § Discussion

    The varying influences on welfare and high levels of inter-correlation emphasise the complex nature of enclosure design.

    “The varying influences on welfare and high levels of inter-correlation emphasise the complex nature of enclosure design.”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation
    § Discussion

    Adaptive management has become well-established as the guiding principle for conservation projects among the world's major conservation NGOs.

    “Adaptive management has become well-established as the guiding principle for conservation projects among the world's major conservation NGOs (Conservation Measures Partnership, 2007).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Conservation Measures Partnership, 2007

      Couldn’t be matched to a paper in Crossref, so it can’t be checked.

  • Probably not a substantial claim: may not pass S2 (checkable), S3 (load-bearing).

    Premisecitation
    § Discussion

    The importance of forming academic links for improved scientific input to zoo management is well established.

    “The importance of forming academic links for improved scientific input to zoo management is well established (Benirschke, 1997; WAZA, 2005).”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites Benirschke, 1997

      Couldn’t be matched to a paper in Crossref, so it can’t be checked.

    • cites WAZA, 2005

      Couldn’t be matched to a paper in Crossref, so it can’t be checked.

66 of 66

  • The paper relies on this without support.

    Swimming is a basic need in penguins.

    “Swimming is a basic need in penguins and may represent an appropriate indicator for enclosure evaluation.”

  • The paper relies on this without support.

    Modern enclosure design is primarily determined using husbandry guidelines.

    “Modern enclosure design is primarily determined using husbandry guidelines, which collate decades of practical experience.”

  • The paper relies on this without support.

    Methods are not standardised for the development of zoo enclosures based on multiple indicators.

    “Methods are not standardised for the development of zoo enclosures based on multiple indicators, and case study species are required.”

  • The paper relies on this without support.

    Penguin behavior in relation to enclosure design has received even less attention than breeding.

    “Penguin behavior in relation to enclosure design has received even less attention than breeding.”

  • The paper relies on this without support.

    Water-use can be subject to seasonal fluctuations.

    “Water-use can be subject to seasonal fluctuations, highlighting the importance of long-term data to mitigate temporal bias.”

  • The paper relies on this without support.

    Food is routinely provided in zoos without requiring penguins to enter the water.

    “Accordingly, where food is routinely provided in zoos without having to enter the water, a deviation from aquatic behavior is expected, though not necessarily a welfare concern.”

  • The paper relies on this without support.

    There are no industry standard criteria to appraise animal enclosures.

    “In the absence of industry standard criteria to appraise animal enclosures, we propose a framework for enclosure design (Fig. 3).”

  • The paper relies on this without support.

    Similar evidence on visitor influence in captive S. humboldti is lacking.

    “However, despite S. humboldti showing a physiological sensitivity to anthropogenic disturbance in the wild (Ellenberg et al., 2006), similar evidence in captivity is lacking, yet desirable.”
8 of 8

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

Each contradiction between two passages listed here was confirmed by an independent check.

  • Figure 1 changes the definition of hatching success

    Major

    The methods define hatching success as the proportion of eggs that hatched. The Figure 1 legend instead requires the chicks to survive to one year, a different breeding outcome.

  • Figure 1 changes the denominator of egg productivity

    Minor

    The methods define egg productivity per female per year, but the Figure 1 legend defines it per colony per year.

  • Figure 2 gives chick productivity an inconsistent denominator

    Minor

    For the comparison plotted in Figure 2, the methods say chick productivity was expressed per penguin rather than per pair. The figure legend instead labels it as chicks per egg.

3 of 3

Cites

Flagged first, then by citations

Research works printed but not linked: 10

  1. Aughtry, 1977, Applied behavioral research at Woodland Park Zoological Gardens, 254
  2. 2014, Penguin (Spheniscidae) care manual
  3. Condon, 2003, The effects of visitors on the behaviour of Humboldt penguins at Chester Zoo, BIAZA Res Newsletter, 4, 3
  4. Edgington, 1990, Penguin management, 49
  5. Hancocks, 2010, Wild mammals in captivity, 121
  6. Hosey, 2013b, Zoo animals, behaviour, management and welfare, 212, 10.1093/hesc/9780199693528.001.0001 · DOI · Paper page
  7. McDonald, 2014, Handbook of biological statistics
  8. Penguin, 2005, Spheniscus penguin husbandry manual: first edition
  9. Sokal, 1995, Biometry: the principles and practices of statistics in biological research
  10. 2005, Building a future for wildlife: the world zoo and aquarium conservation strategy, 1

Cited by

Sorted by citations

Related

Authors
Marshall, A. R., Deere, N. J., Little, H. A., Snipp, R., Goulder, J., & Mayer-Clarke, S.
Affiliations
  • University of York (GB)
  • University of Kent (GB)
Corresponding author
Marshall, Andrew R.
ORCID
Venue
Zoo Biology
Publisher
Wiley
Published
2016-08-03
Volume
35
Issue
5
Pages
385-397
ISSN
0733-3188 (ISSN-L)
DOI
10.1002/zoo.21313
OpenAlex
W2508558843
Semantic Scholar
7dfb4e53990408d2523ead341df871fb3de15b1a
Cited by
33
References
75
Citations by year
2026: 3 · 2025: 3 · 2024: 3 · 2023: 4 · 2022: 8 · 2021: 3 · 2020: 2 · 2019: 3 · 2018: 2 · 2017: 1 · 2016: 1
FWCI
3.29
Type
journal article
Language
en
Open access
closed
Licence
Locations
  • Zoo Biology (publishedVersion)
  • PubMed (publishedVersion)
  • White Rose Research Online (University of Leeds, The University of Sheffield, University of York) (acceptedVersion)
Funders
Aggregates Levy Sustainability Fund
Topics
  • Health Sciences › Veterinary › Small Animals › Animal Behavior and Welfare Studies
  • Physical Sciences › Environmental Science › Ecology › Avian ecology and behavior
  • Life Sciences › Agricultural and Biological Sciences › Ecology, Evolution, Behavior and Systematics › Animal Behavior and Reproduction
Keywords
Humboldt penguin, husbandry, animal welfare, penguin behavior, water consumption, colony age, breeding pairs, conservation breeding
MeSH terms
Animals, Animal Husbandry, Animal Welfare, Animals, Zoo, Behavior, Animal, Breeding, Conservation of Natural Resources, Housing, Animal, Regression Analysis, Reproduction, Spheniscidae

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Claims read by deepseek-v4.1-flash under definition version 3 (extract-v3) on 2026-10-26.

Classified by jev-1.13-20260917 (gold-guideline-v0.2) on 2026-10-26.

Cited sources are checked by gpt-6-sol.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

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