Cited by 32Animal Behavior and Welfare StudiesEffects of Environmental Stressors on LivestockPhysiological and biochemical adaptations

Effect of weather conditions and presence of visitors on adrenocortical activity in captive African penguins (Spheniscus demersus)

Open access
Ozella, L., Anfossi, L., Di Nardo, F., Pessani, D.·2017·General and Comparative Endocrinology

Abstract

A number of potential stressors are present in captive environments and it is critically important to identify them in order to improve health and welfare in ex situ animal populations. In this study, we investigated the adrenocortical activity of a colony of African penguins hosted in an immersive zoo in Italy, with respect to the presence of visitors and local microclimatic conditions, using the non-invasive method of assessing faecal glucocorticoid metabolites (FGMs). The penguins' exhibit is a large naturalistic outdoor enclosure, which closely reproduces the natural habitat of this species. Data collection took place from the beginning of June to the end of August 2014, during the period of maximum flow of visitors. We carried out 12 sampling periods, each involving 2 consecutive days; during the first day we counted the visitors and we registered the meteorological data, and on the second day, we collected the faecal samples, which amounted to a total of 285 faecal samples. Our results showed that the number of visitors did not influence the adrenocortical activity of the African penguins. Conversely, the local microclimatic conditions did influence the physiological stress on these birds. We found that an increase of the daily mean temperature induced a significant increase in FGM concentrations, although humidity and wind speed had a moderating effect on temperature and reduced the heat-induced stress. Moreover, we calculated two climatic indices, commonly used to assess the thermal discomfort in animals, namely the THI (Temperature-Humidity Index) and WCI (Wind Chill Index), and we detected a positive relationship between their values and the FGM levels, demonstrating that these indices could be useful indicators of weather discomfort in African penguins. Our study shows that the simulating naturalistic conditions could have significant benefits for zoo animals, such as reducing the negative effect of visitors. Nevertheless, it should be taken into account where the zoological facility is located and if the local microclimatic conditions are compatible with the hosted species, to ensure that they do not differ greatly from their natural habitat.

AI snapshot

Written from the paper’s full text.

TL;DR

In a captive African penguin colony at an immersive Italian zoo, visitor numbers did not affect faecal glucocorticoid metabolite (FGM) concentrations, but local microclimatic conditions did. Higher mean temperature and higher THI/WCI values were associated with increased FGM levels, while humidity and wind speed moderated temperature-related stress.

Key findings

  • FGM concentrations did not differ by sex (Welch t-test: t = −0.446, p = 0.655), age class (Welch ANOVA: F = 2.196, df = 3, p = 0.097), or time of day (F = 0.638, df = 2, p = 0.530), but did differ significantly between sampling days (F = 2.065, df = 11, p = 0.032).
  • Visitor numbers had no significant effect on FGM levels; the General Linear Model found mean wind speed, mean relative humidity, and instantaneous visitors at observation points (a) and (c) were not significant (F = 11.16, R² = 0.88, p = 0.036).
  • Mean temperature was positively associated with FGM concentrations (p = 0.008), while the interaction terms Temp × Humidity (p = 0.018) and Temp × Wind (p = 0.02) were negatively associated, and Humidity × Wind was positively associated (p = 0.038).
  • THI and WCI were positively related to FGM: THI equation y = 181.96x − 9173.73 (F = 6.388, R² = 0.32, p = 0.03), with +182 ng/g FGM per 1-unit THI increase; WCI equation y = 248.22x − 1788.56 (F = 7.886, R² = 0.38, p = 0.018), with +248 ng/g FGM per 1-unit WCI increase.

Methods

  • Study site: Zoom Torino, Cumiana, Italy; 54 captive African penguins (26 females, 28 males) in a 1500 m² naturalistic outdoor exhibit with a 120 m² pond.
  • Data collection: summer 2014 (2 June–25 August), 12 sampling periods each with 2 consecutive days; day 1 counted visitors and registered meteorological data, day 2 collected faecal samples. The abstract reports 285 faecal samples, while the methods section reports a total of 235 samples.
  • Analysis: FGM measured by validated enzyme immunoassay after methanol:water extraction; Welch t-test/ANOVA, Spearman correlations, PCA, General Linear Model, and simple linear regression for THI and WCI.

Limitations

  • Stated: further research is needed to establish threshold values of climatic indices for African penguins under different management conditions and seasons.
  • Evident: only 12 sampling days in one summer at a single zoo, with FGM averaged at colony level rather than tracking the same individuals across days.
  • Evident: the sample count is inconsistent between the abstract (285) and methods (235), and the study is correlational, so it cannot establish causation.

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

Integrity signals

Registry

Crossref · 10.1016/j.ygcen.2015.12.002

Cites

68 of 68 references verified0 citation errors · 0 not checkable

Statistics

Nothing to recompute.

Claims the paper makes

16 of 60 cited sources checked · 13 supported · 1 flagged · accuracy not yet measured

  • Study design and conductcitation

    The immunoassay was validated for suitability in African penguins by testing specificity, precision, limit of detection, and accuracy.

    “Before FGM analysis, the immunoassay was validated for suitability in African penguins by testing specificity, precision, limit of detection, and accuracy (Anfossi et al., 2014).”
    Quote in the paperSubstantial claim1 of 1 sources checked
    • cites Anfossi et al., 2014 source
  • Findingown data

    FGM concentrations did not differ between age classes of African penguins.

    “age class (Welch one-way ANOVA: F = 2.196, df = 3, p = 0.097)”
    Quote in the paperNot a substantial claim
    • The authors state this as an assumption: FGM concentrations assessed during the day of faecal collection reflected the relative chronic stress accumulated during the previous day.
  • Findingown data

    FGM concentrations did not differ between times of day (morning, afternoon, and evening).

    “or times of day (Welch one-way ANOVA: F = 0.638, df = 2, p = 0.530)”
    Quote in the paperNot a substantial claim
    • The authors state this as an assumption: FGM concentrations assessed during the day of faecal collection reflected the relative chronic stress accumulated during the previous day.
  • Findingown data

    WCI values were positively related to FGM concentrations in the African penguins.

    “The mean FGM concentrations increased as the WCI values increased, and for each 1 unit increment of WCI, there was an increase of 248 ng/g of FGMs”
    • Also stated in: § 4. Discussion · plain
      “we found a positive relationship between daily FGM concentrations and two climatic indices, commonly used in human beings and domestic animals: Temperature-Humidity Index (THI) and Wind Chill Index (WCI).”
    Quote in the paperSubstantial claim
    • The authors state this as an assumption: FGM concentrations assessed during the day of faecal collection reflected the relative chronic stress accumulated during the previous day.
  • Findingown data

    THI values were positively related to FGM concentrations in the African penguins.

    “The mean FGM concentrations increased as the THI values increased, and for each 1 unit increment of THI, we observed an increase of 182 ng/g of FGMs”
    • Also stated in: § 4. Discussion · plain
      “we found a positive relationship between daily FGM concentrations and two climatic indices, commonly used in human beings and domestic animals: Temperature-Humidity Index (THI) and Wind Chill Index (WCI).”
    Quote in the paperSubstantial claim
    • The authors state this as an assumption: FGM concentrations assessed during the day of faecal collection reflected the relative chronic stress accumulated during the previous day.
  • Classified as probably not a substantial claim. 32
  • May combine two claims. 28
  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    The effect of visitors on the welfare of captive animals has been widely studied for more than four decades.

    “While the effect of visitors on the welfare of captive animals has been widely studied for more than four decades (Hosey, 2000;Davey, 2007;Hosey, 2013)”
    Quote in the paperNot a substantial claim1 of 3 sources checked
    • cites Hosey, 2000 source

      The Introduction says the visitor effect was not systematically investigated until comparatively recently, rather than widely studied for more than four decades. The Non-primate studies section also describes published studies of visitor effects on non-primates as virtually non-existent. Page numbers are unavailable in our copy. (LLM, conf=0.87)

      Checked by a reasoning model — may be wrong.

      Experimental — accuracy not yet measured
    • cites Davey, 2007 source
    • cites Hosey, 2013 source
  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Premisecitation

    The African Penguin is an endemic seabird of the coastal region of South Africa and Namibia, and is the only member of the Order Sphenisciformes which breeds in Africa.

    “The African Penguin (Spheniscus demersus) is an endemic seabird of the coastal region of South Africa and Namibia, and is the only member of the Order Sphenisciformes which breeds in Africa (Shelton et al., 1984).”
    Quote in the paperNot a substantial claim1 of 1 sources checked
    • cites Shelton et al., 1984 source
  • Classified as probably not a substantial claim. May combine two claims.

    Premisecitation

    Previous studies have demonstrated that assessing FGMs is useful for detecting and highlighting potentially stressful situations which may influence the welfare of penguins, and it allows detection of individual differences of FGM concentrations.

    “Previous studies have demonstrated that this method is useful for detecting and highlighting potentially stressful situations, which may influence the welfare of penguins, and it allows the detection of individual differences of FGM concentrations (Anfossi et al., 2014;Ozella et al., 2015).”
    Quote in the paperSubstantial claim2 of 2 sources checked
    • cites Anfossi et al., 2014 source
    • cites Ozella et al., 2015 source
  • Classified as probably not a substantial claim.

    Premisecitation

    The physiological stress response in vertebrates results in increased secretion of glucocorticoid hormones subsequent to activation of the HPA axis.

    “The physiological stress response in vertebrates results in an increased secretion of glucocorticoid hormones (GCs) subsequent to the activation of the hypothalamic-pituitaryadrenal (HPA) axis (Möstl and Palme, 2002;Touma and Palme, 2005;Sheriff et al., 2011).”
    Quote in the paperSubstantial claim2 of 3 sources checked
    • cites Möstl and Palme, 2002 source
    • cites Touma and Palme, 2005 source
    • cites Sheriff et al., 2011 source
  • Classified as probably not a substantial claim.

    Study design and conductcitation

    The penguins' diet was not modified throughout the study period to avoid alterations in gut flora and, as a consequence, steroid metabolism.

    “Throughout the study period, the penguins' diet was not modified in order to avoid alterations in gut flora and, as a consequence, steroid metabolism (Sheriff et al., 2011).”
    Quote in the paperSubstantial claim1 of 1 sources checked
    • cites Sheriff et al., 2011 source
  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Study design and conductcitation

    Samples were frozen immediately after collection at −20 °C.

    “Samples were gathered in cryovials and frozen immediately after collection at À20 °C (Millspaugh and Washburn, 2004;Palme et al., 2005;Sheriff et al., 2011).”
    Quote in the paperNot a substantial claim1 of 3 sources checked
    • cites Millspaugh and Washburn, 2004 source
    • cites Palme et al., 2005 source
    • cites Sheriff et al., 2011 source

      The 'Sample collection and storage' section recommends freezing fecal samples immediately after collection. It does not specify −20 °C for those samples or mention cryovials; its recommendation to store at or below −20 °C applies to processed blood samples, not immediate freezing after collection. The paper also does not report that the citing authors' samples were handled this way. (LLM, conf=0.88)

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

    Premisecitation

    A relationship exists between the hypothalamic-pituitary-adrenal (HPA) and hypothalamic-pituitary-gonadal (HPG) axes, and both testosterone and oestrogen modulate the response of the HPA axis.

    “As a relationship exists between the hypothala mic-pituitary-adrenal (HPA) and the hypothalamic-pituitary-go nadal (HPG) axes, and both testosterone and oestrogen modulate the response of the HPA axis (Toufexis et al., 2014)”
    Quote in the paperNot a substantial claim1 of 1 sources checked
    • cites Toufexis et al., 2014 source
  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    A sex-dependent excretion of FGMs exists in certain bird species, such as the European stonechat, Peregrine falcon, and Adelie penguins.

    “Conversely, a sex-dependent excretion of FGMs does exist in certain bird species, such as the European stonechat (Saxicola torquata rubicola) (Goymann, 2005), the Peregrine falcon (Falco peregrinus) (Staley et al., 2007), and the Adelie penguins (Pygoscelis adeliae) (Ninnes et al., 2010).”
    Quote in the paperNot a substantial claim1 of 3 sources checked
    • cites Goymann, 2005 source
    • cites Staley et al., 2007 source
    • cites Ninnes et al., 2010 source
  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Interpretationcitation

    The finding that FGM concentrations did not differ between sexes agreed with results obtained in other avian species, such as the Mourning dove and the Golden eagle.

    “This result agreed with those obtained in other avian species, such as the Mourning dove (Zenzaida macrura) (Washburn et al., 2003) and the Golden eagle (Aquila chrysaetos) (Staley et al., 2007).”
    Quote in the paperNot a substantial claim1 of 2 sources checked
    • cites Washburn et al., 2003 source
    • cites Staley et al., 2007 source
  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Premisecitation

    In gorals, an increase of glucocorticoids was observed during summer months, which could reflect heat stress.

    “In particular, authors observed an increase of glucocorticoids in gorals during the summer months and this result could reflect a form of heat stress in this species (Khonmee et al., 2014).”
    Quote in the paperNot a substantial claim1 of 1 sources checked
    • cites Khonmee et al., 2014 source

      The Results (page not provided) report that summer fecal glucocorticoid concentrations were highest at Night Safari but lowest at Omkoi. The Discussion (page not provided) says the higher summer concentrations at Night Safari could reflect heat stress. The claim omits this facility-specific qualification and implies an increase in gorals generally. (LLM, conf=0.90)

      Experimental — accuracy not yet measured
  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    Recent studies on captive animals such as African lions, Siberian tigers, and gorals show that high temperature could affect animal welfare.

    “A few recent studies on captive animals, such as African lions (Panthera leo), Siberian tigers (Pantera tigris) (Young et al., 2013) and gorals (Naemorhedus griseus) (Khonmee et al., 2014) show that high temperature could affect animal welfare.”
    Quote in the paperNot a substantial claim1 of 2 sources checked
    • cites Young et al., 2013 source
    • cites Khonmee et al., 2014 source
  • May combine two claims.

    Premisecitation

    In this species, FGM levels begin to increase after 5 h from a punctual stress and decrease within 30 h.

    “In a previous study, we demonstrated that in this species the FGM levels begin to increase after 5 h from a punctual stress (i.e.capture and immobilization of animals for 5 min) and decrease within 30 h (Ozella et al., 2015).”
    Quote in the paperSubstantial claim1 of 1 sources checked
    • cites Ozella et al., 2015 source
  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    The effect of weather parameters on glucocorticoid production has been widely studied in various livestock species to assess consequences of stress on productivity.

    “Instead, the effect of weather parameters on glucocorticoid production has been widely studied in various livestock species (Silanikove, 2000), in order to assess the consequences of stress on productivity (Hill and Wall, 2015).”
    Quote in the paperNot a substantial claim1 of 2 sources checked
    • cites Silanikove, 2000 source
    • cites Hill and Wall, 2015 source
  • May combine two claims.

    Findingown data

    The first two components of the PCA explained 99.9% of the whole variance, with PC1 explaining 94.1% and PC2 explaining 5.8%.

    “The first two components of the PCA explained 99.9% of the whole variance (PC1 = 94.1%,PC2 = 5.8%)”
    Quote in the paperNot a substantial claim
  • May combine two claims.

    Findingown data

    Mean temperature and the interaction terms Temp×Humidity, Temp×Wind, and Humidity×Wind affected adrenal activity in the African penguins.

    “The results showed that the factors that affected adrenal activity were the mean temperature and the three factors considered as interaction terms, i.e.Temp ⁄ Humidity, Temp ⁄ Wind, and Humidity ⁄ Wind.”
    Quote in the paperSubstantial claim
    • The authors state this as an assumption: FGM concentrations assessed during the day of faecal collection reflected the relative chronic stress accumulated during the previous day.
  • May combine two claims.

    Findingown data

    Mean FGM concentrations were lower when Temp×Humidity and Temp×Wind increased.

    “FGM concentrations were lower when Temp ⁄ Humidity (p = 0.018), and Temp ⁄ Wind increased (p = 0.02)”
    Quote in the paperSubstantial claim
    • The authors state this as an assumption: FGM concentrations assessed during the day of faecal collection reflected the relative chronic stress accumulated during the previous day.
  • May combine two claims.

    Findingown data

    The average number of instantaneous visitors counted at the wooden footbridge was positively and significantly correlated with the average number of visitors counted at the glass panels and with the daily number of people admitted to the biopark.

    “The average number of instantaneous visitor counted at the wooden footbridge (a) was positively and significantly correlated with the average number of visitors counted at the glass panels (b) (q = 0.78, p = 0.004), and with the daily evaluation of people admitted to the biopark (q = 0.79, p = 0.003).”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Findingown data

    Mean wind speed, mean relative humidity, and mean numbers of instantaneous visitors at observation points (a) and (c) were not significant predictors of FGM concentrations.

    “Conversely, mean wind speed, mean relative humidity, and mean numbers of instantaneous visitors counted at observation points (a) and (c) were not significant (F = 11.16,R 2 = 0.88, p = 0.036).”
    Quote in the paperSubstantial claim
    • The authors state this as an assumption: FGM concentrations assessed during the day of faecal collection reflected the relative chronic stress accumulated during the previous day.
  • May combine two claims.

    Findingown data

    Accumulated rainfall showed very low variability during the observation period, with 0 mm rainfall on 10 of 12 days.

    “The accumulated rainfall showed very low variability during the observation period (the rainfall was 0 mm for 10 days out of 12)”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Findingown data

    Daily mean FGM concentrations varied across the data collection period and significantly differed between sampling days.

    “Daily mean FGM concentrations varied across the data collection period and they significantly differed between sampling days.”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Findingown data

    In this study, FGM levels did not show age-related differences and did not decrease with age.

    “Our results did not show any age-related differences, and there was no decrease in FGM levels with age.”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Findingreasoning

    The interaction between mean temperature and mean relative humidity, as well as the interaction between mean temperature and mean wind speed, showed a negative relationship with FGM concentrations.

    “However, when we considered the interaction between the mean temperature and the mean relative humidity, as well as the mean temperature and the mean wind speed, we observed a negative relationship with FGM concentrations.”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Findingcitation

    Weather factors did not act separately, and their interactions influenced animal welfare in an extremely complex way.

    “As also demonstrated by our results, the weather factors did not act separately, and their interactions influenced animal welfare in an extremely complex way (Van laer et al., 2014).”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Van laer et al., 2014 source
  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Premisereasoning

    African penguins are exhibited in zoos and aquaria all over the world, and as they face an elevated risk of extinction, ex situ conservation programs are becoming increasingly crucial.

    “African penguins are exhibited in zoos and aquaria all over the world, and as they face an elevated risk of extinction, ex situ conservation programs are becoming increasingly crucial.”
    Quote in the paperNot a substantial claim
  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Premisecitation

    The main glucocorticoids produced by the adrenal gland are cortisol and corticosterone, with corticosterone being predominant in birds.

    “The main GCs produced by the adrenal gland are cortisol and corticosterone, with the latter being predominant in birds (Möstl et al., 2005;Palme et al., 2005;Cockrem, 2007).”
    Quote in the paperNot a substantial claim0 of 3 sources checked
    • cites Möstl et al., 2005 source
    • cites Palme et al., 2005 source
    • cites Cockrem, 2007 source
  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Premisecitation

    Gender differences in adrenal activity have been previously reported in several species and may be due to different physiological and behavioural aspects.

    “Gender differences in adrenal activity have been previously reported in several species and may be due to different physiological and behavioural aspects (Touma and Palme, 2005).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Touma and Palme, 2005 source
  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Premisecitation

    If exposure to a stressor persists, chronic GC secretion can lead to deleterious consequences on animal behaviour, individual fitness and reproductive success, and can induce immunosuppression.

    “If exposure to a stressor persists, chronic GC secretion can lead to deleterious consequences on animal behaviour, individual fitness and reproductive success, and can induce immunosuppression (Munck et al., 1984;Liptrap, 1993;Munck and Naráy-Fejes-Tóth, 1994).”
    Quote in the paperNot a substantial claim0 of 3 sources checked
    • cites Munck et al., 1984 source
    • cites Liptrap, 1993 source
    • cites Munck and Naráy-Fejes-Tóth, 1994 source
  • Probably not a substantial claim: may not pass S2 (checkable), S3 (load-bearing), S4 (based).

    Interpretationnone given

    Simulating naturalistic conditions could have significant benefits for zoo animals, such as reducing the negative effect of visitors.

    “Our study shows that the simulating naturalistic conditions could have significant benefits for zoo animals, such as reducing the negative effect of visitors.”
    Quote in the paperNot a substantial claim
  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Premisecitation

    The current conservation status of the African penguin is Endangered, and the wild population has decreased to less than 75,000-80,000 mature individuals.

    “The current conservation status of this species is ''Endangered”
    • Also stated in: § 1. Introduction · plain
      “The population in the wild of this species has dramatically decreased in recent years to less than 75,000-80,000 mature individuals (BirdLife International, 2013).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites BirdLife International, 2013

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

  • May combine two claims.

    Premisecitation

    The non-invasive method of faecal hormone sampling permits monitoring of the animal's endocrine status without capturing or handling the animals, which may compromise accurate assessment of stress.

    “This non-invasive method permits the monitoring of the animal's endocrine status without the necessity to capture or handle the animals, which may compromise the accurate assessment of stress (Millspaugh and Washburn, 2004;Goymann, 2012).”
    Quote in the paperSubstantial claim0 of 2 sources checked
    • cites Millspaugh and Washburn, 2004 source
    • cites Goymann, 2012 source
  • Classified as probably not a substantial claim.

    Study design and conductcitation

    Sample collection took place immediately after defecation to avoid bacterial and microbial degradation.

    “Sample collection took place immediately after defecation to avoid bacterial and microbial degradation (Millspaugh and Washburn, 2004).”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Millspaugh and Washburn, 2004 source
  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Interpretationreasoning

    Gender differences in FGMs could vary depending on the biological stage of birds, such as breeding period.

    “gender differences in FGMs could vary depending on the biological stage of birds, such as breeding period.”
    Quote in the paperNot a substantial claim
  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    Monitoring adrenal activity through non-invasive faecal hormone sampling is rapidly gaining popularity as a tool to assess zoo animal welfare.

    “Monitoring adrenal activity through non-invasive faecal hormone sampling is rapidly gaining popularity as a tool to assess zoo animal welfare (Clark et al., 2012)”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Clark et al., 2012 source
  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Premisecitation

    African penguins start to become heat-stressed at air temperatures of 24 °C, when they have been observed panting, a behavioural adaptation to increase heat release with respiratory evaporation.

    “Indeed, African penguins start to become heat-stressed at air temperatures of 24 °C, when they have been observed panting (Frost et al., 1976), a behavioural adaptation to increase heat release with respiratory evaporation.”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Frost et al., 1976 source
  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    The zoo exhibit design influences the well-being of captive animals.

    “Particularly, it is known that the zoo exhibit design influences the well-being of captive animals (Morgan and Tromborg, 2007;Young et al., 2013).”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites Morgan and Tromborg, 2007 source
    • cites Young et al., 2013 source
  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    The absence of a visible physical barrier fosters a more positive attitude by the public towards the animals.

    “At the same time, the absence of a visible physical barrier fosters a more positive attitude by the public towards the animals (Tofield et al., 2003).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Tofield et al., 2003 source
  • Classified as probably not a substantial claim.

    Premisecitation

    Animals in zoos are often subjected to microclimatic conditions that can differ greatly from their natural habitat, and to which their species is not usually adapted.

    “Moreover, animals in zoos are often subjected to microclimatic conditions that can differ greatly from their natural habitat, and to which their species is not usually adapted (Morgan and Tromborg, 2007).”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Morgan and Tromborg, 2007 source
  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    Removal or reduction of physical barriers and safety mechanisms in naturalistic exhibits leaves animals unprotected from direct trauma and injuries due to irresponsible visitor behaviour or wild animal predators.

    “For example, the removal or reduction of the physical barriers and the safety mechanisms leave animals unprotected from direct trauma and injuries due to irresponsible visitor behaviour or wild animal predators (Sha et al., 2013).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Sha et al., 2013

      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). May combine two claims.

    Interpretationcitation

    Naturalistic exhibits may allow animals greater freedom of movement, enhancing choice and control over interactions with visitors, which may reduce negative impacts from the public.

    “It is possible that naturalistic exhibits allow animals greater freedom of movement, enhancing choice and control over their interactions with visitors (Davey, 2007), which may reduce potentially negative impacts from the public.”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Davey, 2007 source
  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Premisecitation

    In order to adapt to hot climates, African penguins breed in burrows dug in guano, which maintains a constant microclimate, with high relative humidity, buffered temperatures and little exposure to the wind.

    “Moreover, in order to adapt to hot climates, these penguins breed in burrows dug in guano, which maintains a constant microclimate, with high relative humidity, buffered temperatures and little exposure to the wind (Frost et al., 1976).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Frost et al., 1976 source
  • May combine two claims.

    Interpretationcitation

    The FGM levels obtained in this study represent a pooled measure over a certain time period, reflecting cumulative secretion.

    “Consequently, we consider the FGM levels obtained as a pooled measure over a certain time period, representing a cumulative secretion, as suggested by several other authors (e.g.Goymann et al., 1999;Palme, 2005;Keay et al., 2006;Cockrem, 2007;Palme, 2012).”
    Quote in the paperSubstantial claim0 of 3 sources checked
    • cites Goymann et al., 1999 source
    • cites Palme, 2005 source
    • cites Keay et al., 2006 source
  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Premisecitation

    According to Köppen and Geiger (1930), the climate of Simon's Town is temperate-humid, classified as Csb: mesothermal with temperatures in the warmest month being less than 22 °C.

    “According to Köppen and Geiger (1930), the climate of Simon's Town is temperate-humid, and is classified as Csb: mesothermal with temperatures in the warmest month being less than 22 °C.”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Köppen and Geiger (1930)

      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.

    Interpretationown data

    Monitoring of FGMs is a valuable tool for advancing understanding of adrenal function and stress responses in captive animals, and can enhance ex situ management of threatened species.

    “In conclusion, our study has shown that monitoring of FGMs is a valuable tool for advancing our understanding of adrenal function and stress responses in captive animals, and can enhance ex situ management of threatened species.”
    Quote in the paperNot a substantial claim
  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Premisecitation

    The exhibit design of naturalistic zoos simulates the natural habitats of animals, thus providing direct benefit to captive animals by promoting naturalistic behaviour.

    “The exhibit design of naturalistic zoos simulates the natural habitats of animals, thus providing direct benefit to captive animals by promoting naturalistic behaviour (Sha et al., 2013).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Sha et al., 2013

      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

    High ambient temperature, wind speed and humidity are recognized as environmental stressing factors for farm animals.

    “In particular, high ambient temperature, wind speed and humidity are recognized as environmental stressing factors for farm animals (Silanikove, 2000).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Silanikove, 2000 source
45 of 45
  • The authors state this as an assumption.

    FGM concentrations assessed during the day of faecal collection reflected the relative chronic stress accumulated during the previous day.

    “Therefore, we assume that FGM concentrations assessed during the day of faecal collection reflected the relative chronic stress accumulated during the previous day.”
  • The paper relies on this without support.

    Meteorological data from the ARPA Piemonte station about 1 km from the penguins' exhibit represent the microclimatic conditions experienced by the penguins.

    “The meteorological data were obtained from the meteorological station of ''ARPA Piemonte”
  • The paper relies on this without support.

    Naturalistic exhibits are commonly large outdoor areas, so animals are greatly exposed to surrounding environments and local microclimate.

    “Furthermore, as the naturalistic exhibits are commonly large outdoor areas, animals are greatly exposed to surrounding environments, as well as to the local microclimate.”
3 of 3

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?

  • Penguins are a common zoo-housed species, especially little penguins in Australian zoos.

    “Limited research has been conducted to examine the effects of visitors on zoo-housed penguins despite penguins being a commonly housed zoo species, especially little penguins (Eudyptula minor) in Australian zoos [3,10,11,12,13,14,15].”

    From Effect of Covering a Visitor Viewing Area Window on the Behaviour of Zoo-Housed Little Penguins (Eudyptula minor) (2020) · cites this paper as [15]

    The Introduction says African penguins are exhibited in zoos and aquaria worldwide, supporting the general point that penguins are zoo-housed. It does not establish that penguins are commonly housed overall or that little penguins are especially common in Australian zoos; the study concerns African penguins at an Italian zoo (Study site and animals). (LLM, conf=0.86)

    Experimental — accuracy not yet measured

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.

  • Conflicting total numbers of faecal samples

    Major

    The abstract reports 285 faecal samples, but the collection methods report a total of 235. The paper does not explain the 50-sample difference.

1 of 1

Cites

Flagged first, then by citations

1 of the 69 references couldn’t be matched to a known paper.

Cited by

Sorted by citations

Authors
Ozella, L., Anfossi, L., Di Nardo, F., & Pessani, D.
Affiliations
University of Turin (IT)
Corresponding author
Ozella, L.
Venue
General and Comparative Endocrinology
Publisher
Elsevier BV
Published
2017-02
Volume
242
Pages
49-58
ISSN
0016-6480 (ISSN-L)
OpenAlex
W2195908993
Cited by
32
References
69
Citations by year
2026: 2 · 2025: 3 · 2024: 2 · 2023: 4 · 2022: 3 · 2021: 4 · 2020: 7 · 2018: 6 · 2016: 1
FWCI
3.74
Type
journal article
Language
en
Open access
Locations
  • General and Comparative Endocrinology (publishedVersion)
  • PubMed (publishedVersion)
  • Institutional Research Information System University of Turin (University of Turin) (submittedVersion, other-oa)
Funders
Advanced Research Projects Agency
Topics
  • Health Sciences › Veterinary › Small Animals › Animal Behavior and Welfare Studies
  • Life Sciences › Agricultural and Biological Sciences › Animal Science and Zoology › Effects of Environmental Stressors on Livestock
  • Physical Sciences › Environmental Science › Ecology › Physiological and biochemical adaptations
Keywords
African penguin, Spheniscus demersus, adrenocortical function, fecal glucocorticoid metabolites, microclimate, heat stress, temperature-humidity index, wind chill index, zoo animal welfare, captive birds, thermal discomfort
MeSH terms
Adrenal Glands, Animals, Animals, Zoo, Feces, Glucocorticoids, Reproduction, Stress, Physiological, Weather, 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 2026-10-27.

Classified by jev-1.13-20260917 (gold-guideline-v0.2) on 2026-10-27.

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.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review