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Cited by 8Animal Behavior and Welfare StudiesAvian ecology and behaviorMarine animal studies overview

The Benefits of Increased Space and Habitat Complexity for the Welfare of Zoo-Housed King Penguins (Aptenodytes patagonicus)

Open access
Fuller, Grace, Jones, Megan, Gartland, Kylen N., Zalewski, Sara, Heintz, Matthew R., Allard, Stephanie·2023·Animals
DOI 10.3390/ani13142312PMC PMC10376525
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Abstract

Zoos and aquariums accredited by the Association of Zoos and Aquariums embrace animal welfare as a foundational principle of habitat design. Modern habitats are designed to provide animals with choices and agency over their environment, and to encourage species-appropriate behavior and space use. In 2016, the Detroit Zoological Society opened the Polk Penguin Conservation Center, a 3065.80 m2 facility that features a naturalistic design. The building was designed to optimize animal welfare by incorporating various substrates, nesting sites, and a 1234 kL pool with elements of underwater complexity. The facility houses a mixed-species group of penguins that were previously housed in a smaller habitat that opened in 1968. Between 2015 and 2022, we opportunistically monitored the behavior of ten king penguins (Aptenodytes patagonicus) as they moved back and forth between the two buildings while additional modifications were made to the new habitat. We collected 695 h of behavioral observations and 10,416 h of data from flipper-mounted time–depth recorders. We found that the king penguins spent less time engaged in aggression and more time engaged in swimming and positive social behaviors in the redesigned space. They also spent less time in proximity to other species of penguins and more time alone. These behavioral trends suggest that increased space and environmental complexity had positive welfare benefits for these penguins.

AI snapshot

Written from the paper’s full text.

TL;DR

A post-occupancy evaluation of ten zoo-housed king penguins found that moving between the Detroit Zoo’s older Penguinarium and the larger, more complex Polk Penguin Conservation Center was associated with more swimming, more positive social behavior, and less aggression. The authors conclude that increased space and habitat complexity had positive welfare benefits, though size and complexity could not be disentangled.

Key findings

  • Time–depth recorder data showed an approximately threefold increase in time spent swimming in the PPCC compared with the Penguinarium; observational data indicated a three- to fourfold increase, and every individual increased swimming to some degree.
  • The penguins spent significantly less time walking and significantly more time laying in the PPCC; feeding trended higher in the PPCC, and bathing rates were significantly higher there.
  • Total agonism, given agonism, and received agonism were significantly higher in the Penguinarium across both study phases; total agonism per hour ranged from 2.70 ± 3.13 to 13.04 ± 6.67 in the Penguinarium and from 1.29 ± 1.02 to 5.79 ± 4.32 in the PPCC.
  • Allopreening and displays were higher in the PPCC in Phase 1, but in Phase 2 allopreening did not differ significantly and displays were higher in the Penguinarium; the penguins also spent less time in proximity to other species and more time alone in the PPCC.

Methods

  • Post-occupancy evaluation at the Detroit Zoo using 10 king penguins in a mixed-species colony, comparing the Penguinarium (opened 1968; ~132.5 kL pool, 1.8 m deep) and the PPCC (opened 2016; 3065.80 m² facility, 1234 kL pool, 7.6 m deep) as penguins moved back and forth during 2015–2017 and 2019–2022.
  • Behavioral observations used instantaneous scan sampling at one-minute intervals plus all-occurrence event recording; analyses covered 694.8 h (5368 observations: 311.9 h in the Penguinarium, 382.9 h in the PPCC), with 40 observers maintaining reliability above 90%.
  • Flipper-mounted LAT1800L time–depth recorders recorded pressure and wet/dry state every six seconds, yielding 10,416 h of data; each penguin wore a TDR four times for a mean of 16.20 ± 1.24 days per deployment. Analyses used Wilcoxon two-sample tests with Monte Carlo permutations and generalized linear mixed models with habitat, sex, age, time of day, and season as predictors.

Limitations

  • The paper states that because the PPCC is both substantially larger and more complex than the Penguinarium, it is not possible to tease apart the relative contributions of habitat size versus complexity.
  • The authors note that a single-group POE makes it difficult to differentiate individual, group-level, and species trends, and to rule out changing social dynamics or passage of time as confounds; they also did not identify individuals in proximity, so social networks and pair bonds could not be assessed.
  • The text makes evident additional constraints: opportunistic monitoring across two phases with changing subjects and colony composition, habitat modifications between phases, possible visibility differences between habitats, and temperature differences that could not be ruled out.

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

Integrity signals

Registry

Crossref · 10.3390/ani13142312

Cites

51 of 51 references verified0 citation errors · 0 not checkable

Statistics

Nothing to recompute.

Claims the paper makes

8 of 25 cited sources checked · 2 supported · 1 flagged · accuracy not yet measured

  • Premisecitation

    Increases in exhibit complexity and size have been shown to positively impact behavioral patterns in diverse taxa.

    “However, increases in exhibit complexity and size have been shown to positively impact behavioral patterns in diverse taxa.”
    Quote in the paperSubstantial claim2 of 2 sources checked
    • cites [7] Lawrence, K., Sherwen, S.L., and Larsen, H. (2021). Natural Habitat Design for Zoo-Housed Elasmobranch and Teleost Fish Species Improves Behavioural Repertoire and Space Use in a Visitor Facing Exhibit. Animals, 11. source

      The Introduction describes positive behavioural effects of enriched, more naturalistic enclosures in primates, sitatunga and leopards, and the Conclusions report increased natural behaviours in the fish studied. The paper supports the complexity and diverse-taxa portions of the claim, but the passages do not show that increasing exhibit size improves behaviour; its renovation added habitat features, not exhibit space. (LLM, conf=0.86)

      Experimental — accuracy not yet measured
    • cites [8] Ellis, 2022, An Improvement in Enclosure Design Can Positively Impact Welfare, Reduce Aggressiveness and Stabilise Hierarchy in Captive Galapagos Giant Tortoises, J. Zool. Bot. Gard. source

      The Introduction (page unavailable) says environmental enrichment and available space contribute to well-being across a wide range of animal taxa. The Discussion (page unavailable) reports improved welfare and reduced aggression after tortoises moved to a more resource-rich enclosure. The paper therefore supports the general benefit of larger, enriched exhibits, but its evidence for improved behavioral patterns is specific to tortoises, not diverse taxa. (LLM, conf=0.82)

      Experimental — accuracy not yet measured
  • Premisecitation

    Pool use may indicate a better welfare state for captive penguins.

    “Pool use may indicate a better welfare state for captive penguins.”
    Quote in the paperSubstantial claim1 of 2 sources checked
    • cites [21] Reisfeld, 2013, Reducing bumblefoot lesions in a group of captive Magellanic penguins (Spheniscus magellanicus) with the use of environmental enrichment, Pesqui. Vet. Bras. source
    • cites [22] Blay, 2001, Optimal conditions for breeding of captive Humboldt penguins (Spheniscus humboldti): A survey of British zoos, Zoo Biol. source
  • Findingown data

    King penguins engaged in more positive social behaviors (such as species-typical displays and allopreening) in the PPCC than in the Penguinarium.

    “They also engaged in more positive social behaviors, such as species-typical displays and allopreening, and fewer aggressive behaviors in the PPCC.”
    • Also stated in: § Abstract · plain
      “We found that the king penguins spent less time engaged in aggression and more time engaged in swimming and positive social behaviors in the redesigned space.”
    Quote in the paperSubstantial claim
  • Findingown data

    The percentage of time spent in proximity to another king penguin did not vary between habitats across both phases.

    “The percentage of time spent in proximity to another king penguin did not vary between habitats across both phases (Table 5).”
    Quote in the paperNot a substantial claim
  • Findingown data

    Based on TDR data, the penguins spent more time swimming at the surface in the Penguinarium than in the PPCC.

    “Based on TDR data, the penguins spent more time swimming at the surface in the Penguinarium than in the PPCC (Table 4; Figure 4).”
    Quote in the paperNot a substantial claim
  • May combine two claims. 50
  • Classified as probably not a substantial claim. 34
  • The quote only partly states this claim. 2

  • May combine two claims.

    Findingcitation

    Like their wild counterparts, the penguins swam the most during the non-breeding season, followed by the breeding season, with the least swimming occurring around molt.

    “Like their wild counterparts, they swam the most during the non-breeding season [27], followed by the breeding season, with the least swimming occurring around molt [29].”
    Quote in the paperSubstantial claim1 of 2 sources checked
    • cites [27] Charrassin, 2001, Utilisation of the oceanic habitat by king penguins over the annual cycle, Mar. Ecol. Prog. Ser. source

      The citation [27] is attached to the claim that wild penguins swam most during the non-breeding season. The Winter crèche section says distances covered were highest in winter, while Birds and study periods says those winter birds were caring for chicks—so the reported peak was during chick rearing, not a non-breeding period. The later comparison with breeding and molt is attached to [29], not this source. (LLM, conf=0.87)

      Checked by a reasoning model — may be wrong.

      Experimental — accuracy not yet measured
    • cites [29] Groscolas, 1992, How to molt while fasting in the cold—The metabolic and hormonal adaptations of emperor and king penguins, Ornis Scand. source

  • Classified as probably not a substantial claim.

    Premisecitation

    Magellanic penguins that spend more time in water have a reduced incidence of pododermatitis.

    “Magellanic penguins that spend more time in water have a reduced incidence of pododermatitis (commonly known as bumblefoot) [21]”
    Quote in the paperSubstantial claim1 of 1 sources checked
    • cites [21] Reisfeld, 2013, Reducing bumblefoot lesions in a group of captive Magellanic penguins (Spheniscus magellanicus) with the use of environmental enrichment, Pesqui. Vet. Bras. source

      The Discussion reports that increased time in water was associated with smaller existing bumblefoot lesions in four of five captive Magellanic penguins, and suggests aquatic activity may help prevent bumblefoot. It did not measure incidence of new cases: all five penguins already had lesions, so the claim's incidence wording goes beyond the observed result. (LLM, conf=0.86)

      Experimental — accuracy not yet measured

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

    Findingown data

    The most frequent behavior observed was standing.

    “The most frequent behavior we observed was standing, which is consistent with penguins in other studies [17,46,47].”
    Quote in the paperNot a substantial claim2 of 3 sources checked
    • cites [17] Marshall, 2016, Husbandry and enclosure influences on penguin behavior and conservation breeding, Zoo Biol. source

      The Results (Table II; page unavailable) show resting was common in the penguin colonies, which lends some support to the comparison with other studies. But the table does not distinguish standing from lying while resting, and the ethogram (page unavailable) defines both separately. The source therefore does not establish that standing was the most frequent behavior. (LLM, conf=0.82)

      Experimental — accuracy not yet measured
    • cites [46] Foerder, 2013, Behavioural synchrony in two species of communally housed captive penguins, Behaviour source
    • cites [47] Galante, J., and Margulis, S.W. (2022). Comparing Data Collection Tools for Zoo Management Decision-Making: A Case Study Examining Behavioral Measures of Humboldt Penguin Bond Strength. Animals, 12. source

      The cited paper’s Results (§3.1, page unavailable) report standing among the penguins’ recorded activities and say one pair spent significantly more time standing than other individuals. They do not establish that standing was the most frequent behavior overall, so the paper supports the comparison only in part. (LLM, conf=0.78)

      Experimental — accuracy not yet measured

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

    Premisecitation

    Pool use in Humboldt penguins was correlated with available land space across European zoos.

    “Pool use in Humboldt penguins (Spheniscus humboldti) was correlated with available land space across European zoos [17]”
    Quote in the paperNot a substantial claim1 of 1 sources checked
    • cites [17] Marshall, 2016, Husbandry and enclosure influences on penguin behavior and conservation breeding, Zoo Biol. source

  • May combine two claims.

    Findingown data

    The GLMMs demonstrated that swimming increased in the PPCC across all seasons but decreased during the molting season regardless of habitat.

    “The GLMMs further demonstrated that swimming increased in the PPCC across all seasons but decreased during the molting season regardless of habitat (Table 7).”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Findingown data

    The all-occurrence rate of allopreening was significantly higher in the PPCC in Phase 1, but the difference between habitats was non-significant in Phase 2.

    “The all-occurrence rate of allopreening was significantly higher in the PPCC in Phase 1, but the difference between habitats was non-significant in Phase 2 (Table 5).”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Findingown data

    In the total dataset, feeding behavior was no longer significant and rather trended towards significance.

    “However, feeding behavior was no longer significant and rather trended towards significance, and proximity to another king penguin became significant (Table 6).”
    Quote in the paperNot a substantial claim

  • The quote only partly states this claim.

    Findingown data

    King penguins spent more time alone in the PPCC than in the Penguinarium.

    “They also spent less time in proximity to other species of penguins and more time alone.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Findingown data

    The percentage of time spent alone was significantly higher in the Penguinarium in Phase 1, but the difference between habitats was non-significant in Phase 2.

    “The percentage of time spent alone was significantly higher in the Penguinarium in Phase 1, but the difference between habitats was non-significant in Phase 2 (Table 5).”
    Quote in the paperNot a substantial claim

  • The quote only partly states this claim.

    Findingown data

    King penguins spent less time in proximity to other species of penguins in the PPCC than in the Penguinarium.

    “They also spent less time in proximity to other species of penguins and more time alone.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Findingown data

    The percentage of time spent in proximity to a penguin from another species did not vary between habitats in Phase 1 but was significantly higher in the Penguinarium in Phase 2.

    “The percentage of time spent in proximity to a penguin from another species did not vary between habitats in Phase 1 but was significantly higher in the Penguinarium in Phase 2 (Table 5).”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Findingown data

    In the Penguinarium, the penguins tended to form a line and continuously walk around the perimeter of the circular land space, a behavior that was not as pronounced in the larger PPCC.

    “In the Penguinarium, the penguins tended to form a line and continuously walk around the perimeter of the circular land space, a behavior that was not as pronounced in the larger PPCC.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Findingown data

    The change in allopreening was not sustained in Phase 2, and the penguins displayed more in the Penguinarium in Phase 2.

    “However, the change in allopreening was not sustained in Phase 2, and the penguins displayed more in the Penguinarium in Phase 2.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Findingnone given

    Chicks were present in both habitats in Phase 2 of the study, but the highest rates of agonistic behavior occurred in the Penguinarium in Phase 1.

    “Chicks were present in both habitats in Phase 2 of the study, but the highest rates of agonistic behavior occurred in the Penguinarium in Phase 1.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Findingreasoning

    The penguins did not spend much time swimming below 6 m, suggesting that the pool floor was not an appealing location for them.

    “However, they did not spend much time swimming below 6 m, suggesting that the pool floor was not an appealing location for them.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Findingown data

    Overall rates of agonistic behavior were highest during the breeding season in both habitats but were higher in the Penguinarium compared to in the PPCC.

    “Overall rates of agonistic behavior were highest during the breeding season in both habitats but were higher in the Penguinarium compared to in the PPCC.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Findingown data

    We observed the penguins in both habitats during periods when they were closed to visitors, and swimming patterns remained unchanged.

    “Although we did not systematically assess visitor numbers, we observed the penguins in both habitats during periods when they were closed to visitors, and swimming patterns remained unchanged.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Findingown data

    Regardless of habitat, the king penguins spent most of their time in proximity to other king penguins, followed by time alone, with the least time spent in proximity to allospecifics.

    “Regardless of habitat, the king penguins spent most of their time in proximity to other king penguins, followed by time alone, with the least time spent in proximity to allospecifics.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Findingnone given

    This trend was consistent for both study phases and across both agonistic directionalities (given and received).

    “This trend was consistent for both study phases and across both agonistic directionalities (given and received).”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Findingown data

    When given the opportunity, the penguins spent less time swimming at the water surface and increased their time swimming at depths greater than 2 m.

    “When given the opportunity, the penguins spent less time swimming at the water surface and increased their time swimming at depths greater than 2 m, suggesting that deeper pools are preferred by this larger penguin species.”
    Quote in the paperSubstantial claim

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

    Findingown data

    Feeding was one of the few behaviors that showed a significant sex difference in this study, with females spending more time feeding.

    “Feeding was one of the few behaviors that showed a significant sex difference in this study, with females spending more time feeding.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Findingown data

    The average rates of given agonism, received agonism, and total agonism were all significantly higher in the Penguinarium than in the PPCC.

    “The average rate of given agonism, received agonism, and total agonism were all significantly higher in the Penguinarium (Table 6; Figure 7).”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Findingreasoning

    An additional 20 gentoos were added to the group after the initial move to the PPCC, but overall social density may not have increased that much due to the size of the PPCC habitat.

    “An additional 20 gentoos were added to the group after the initial move to the PPCC, but overall social density may not have increased that much due to the size of the PPCC habitat.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Findingown data

    Positive social behaviors (both allopreening and displaying) increased in the PPCC in Phase 1, supporting the initial prediction.

    “Positive social behaviors (both allopreening and displaying) increased in the PPCC in Phase 1, supporting our initial prediction.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Findingown data

    Six individuals displayed decreased proximity to penguins from other species while four demonstrated increased proximity.

    “Similarly, six individuals displayed decreased proximity to penguins from other species while four demonstrated increased proximity (Figure 9).”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Findingown data

    The mixed model showed fewer displays overall during the breeding season compared to the nonbreeding season, with the highest rate of displays occurring during molt.

    “Surprisingly, the mixed model showed fewer displays overall during the breeding season compared to the nonbreeding season, with the highest rate of displays occurring during molt.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Findingown data

    Lola chose not to swim in either habitat and suffered from medical problems that caused chronic lameness.

    “Lola, who chose not to swim in either habitat, suffered from medical problems that caused chronic lameness.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Findingown data

    At the individual level, six individuals demonstrated increased proximity to other king penguins when in the PPCC, but four demonstrated decreased proximity.

    “At the individual level, six individuals demonstrated increased proximity to other king penguins when in the PPCC, but four demonstrated decreased proximity (Figure 8).”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Findingown data

    The penguins showed an increase in positive social behavior and engaged in less agonistic behavior.

    “We did see an increase in positive social behavior, and the penguins engaged in less agonistic behavior.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Findingown data

    Habitat, season, and time of day were all variables that significantly influenced rates of all-occurrence agonism.

    “The GLMM demonstrated that habitat, season, and time of day were all variables that significantly influenced rates of all-occurrence agonism (Table 7).”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Findingown data

    Walking behavior showed a seasonal effect, with less walking during molt and more during the breeding season.

    “Walking behavior also showed a seasonal effect, with less walking during molt (when the penguins tended to stand in place) and more during the breeding season.”
    Quote in the paperNot a substantial claim

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

    Findingown data

    Although there was a slight increase in feeding in the PPCC, we rarely observed this behavior.

    “Although there was a slight increase in feeding in the PPCC, we rarely observed this behavior.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Findingnone given

    Some individuals, such as King 23, Arthur, and Gertie, hardly swam at all in the Penguinarium, making the increase in swimming in the PPCC particularly dramatic.

    “Some individuals, such as King 23, Arthur, and Gertie, hardly swam at all in the Penguinarium, making the increase in swimming in the PPCC particularly dramatic.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Findingown data

    The penguins engaged in more bathing behaviors in the PPCC, and they tended to perform these preening and adjusting movements more during the non-breeding season.

    “The penguins also engaged in more bathing behaviors in the PPCC, and they tended to perform these preening and adjusting movements more during the non-breeding season, when they were already swimming more.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Findingown data

    They increased their time spent laying in the Penguinarium during the second phase of the study, when the Penguinarium also contained an ice machine.

    “Furthermore, they increased their time spent laying in the Penguinarium during the second phase of the study, when the Penguinarium also contained an ice machine.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Findingown data

    In the PPCC, several penguins showed a preference for floating in the water column above the bubbler, which was one of several complex elements not available in the Penguinarium pool.

    “In the PPCC, several of the penguins showed a preference for floating in the water column above the bubbler, which was one of several complex elements not available in the Penguinarium pool.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Findingown data

    The TDR data showed that swimming in this study coincided with day-phase lighting in both habitats, suggesting these penguins did not utilize the pool in darkness.

    “The TDR data showed that swimming in this study coincided with day-phase lighting in both habitats, suggesting these penguins did not utilize the pool in darkness.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Findingnone given

    Some individuals consistently changed their proximity both to king penguins and other species between the two habitats, whereas other individuals showed opposite trends depending on the identity of the species in proximity.

    “Some individuals consistently changed their proximity both to king penguins and other species between the two habitats, whereas other individuals showed opposite trends depending on the identity of the species in proximity.”
    Quote in the paperNot a substantial claim

  • Classified as probably not a substantial claim.

    Study design and conductnone given

    Only observations with a minimum of 50% behavioral visibility were considered sufficient for inclusion in analyses.

    “Only observations with a minimum of 50% behavioral visibility were considered sufficient for inclusion in analyses.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Study design and conductcitation

    Wearing the TDRs coincided with only minor changes in the behavior of the penguins, with no welfare concerns.

    “We have previously demonstrated that wearing the TDRs coincided with only minor changes in the behavior of the penguins, with no welfare concerns [35].”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [35] Fuller, 2019, Validation and welfare assessment of flipper-mounted time-depth recorders for monitoring penguins in zoos and aquariums, Appl. Anim. Behav. Sci. source

  • Classified as probably not a substantial claim.

    Study design and conductown data

    All observers maintained reliability above 90% based on the mean percentage difference calculated on tandem observations, reassessed quarterly.

    “All observers maintained reliability above 90% based on the mean percentage difference calculated on tandem observations, and this criterion was reassessed quarterly for all observers.”
    Quote in the paperSubstantial claim

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

    Study design and conductnone given

    Each observer passed a three-part reliability test, including identification, ethogram, and tandem observations.

    “Each observer passed a three-part reliability test, which included an identification test for all focal penguins, a multiple-choice test covering the ethogram, and three observations scored in tandem with one of the principal investigators.”
    Quote in the paperSubstantial claim

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

    Study design and conductown data

    The weight of the TDR in air with the cradle was less than 0.2% of the body weight of the smallest king penguin in the study.

    “The weight of the TDR in air with the cradle is 14.1 g, which was less than 0.2% of the body weight of the smallest king penguin in the study.”
    Quote in the paperNot a substantial claim

  • Classified as probably not a substantial claim.

    Study design and conductnone given

    The exact dates that an individual penguin wore a TDR were matched between the two habitats.

    “The exact dates that an individual penguin wore a TDR were matched between the two habitats.”
    Quote in the paperSubstantial claim

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

    Study design and conductnone given

    The study was approved by the DZS's Animal Welfare and Management Committee.

    “This study was conducted at the Detroit Zoo in Royal Oak, Michigan, U.S.A., and was approved by the DZS’s Animal Welfare and Management Committee.”
    Quote in the paperNot a substantial claim

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

    Premisecitation

    Magellanic penguins spent more time swimming after their pool was changed from freshwater to saltwater.

    “whereas Magellanic penguins (S. magellanicus) spent more time swimming after their pool was changed from freshwater to saltwater [18].”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [18] Reisfeld, 2013, Behavioral Responses of Magellanic Penguins (Spheniscus magellanicus) (Foster) to Saltwater Versus Freshwater, Zoo Biol. source

  • May combine two claims.

    Premisecitation

    POEs remain relatively rare in the scientific literature, with existing studies showing a taxonomic bias towards mammals.

    “In spite of their great potential to inform exhibit design, POEs remain relatively rare in the scientific literature, with existing studies showing a taxonomic bias towards mammals [1].”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [1] Kelling, 2011, Postoccupancy evaluations in zoological settings, Zoo Biol. source

  • May combine two claims.

    Interpretationreasoning

    Given the choice, king penguins seem to prefer an open water surface and depths extending to 6 m.

    “Given the choice, king penguins seem to prefer an open water surface and depths extending to 6 m.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Interpretationreasoning

    It seems as if the penguins' overall activity level remained the same, whereas the preferred venue-land or water-changed with the habitat.

    “It seems as if their overall activity level remained the same, whereas the preferred venue—land or water—changed with the habitat.”
    Quote in the paperNot a substantial claim

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

    Study design and conductown data

    Time spent investigating and performing other rarer behaviors did not occur frequently enough to analyze statistically.

    “Time spent investigating and performing other rarer behaviors (which we lumped as “other”) did not occur frequently enough to analyze statistically.”
    Quote in the paperNot a substantial claim

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

    Study design and conductreasoning

    The study ran Wilcoxon two-sample tests on both the total combined dataset and the data for phases 1 and 2 separately to ensure coherence.

    “Given that the study occurred in two distinct phases, we ran the Wilcoxon two-sample tests on both the total combined dataset and the data for phases 1 and 2 separately to ensure coherence.”
    Quote in the paperNot a substantial claim

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

    Premisecitation

    The first zoo POEs noted dramatic changes in behavior associated with moving great apes from 20th-century "hard" zoo architecture to naturalistic enclosures, in which rates of agonistic and abnormal behaviors declined precipitously.

    “The first zoo POEs noted dramatic changes in behavior associated with moving great apes from 20th-century “hard” zoo architecture to naturalistic enclosures, in which rates of agonistic and abnormal behaviors declined precipitously [3].”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [3] Maple, 1987, Post-occupancy evaluation in the zoo, Appl. Anim. Behav. Sci. source

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

    Premisecitation

    Providing zoo-housed Humboldt penguins with a mock whale skeleton increased the amount of time they spent swimming.

    “Providing zoo-housed Humboldt penguins with a mock whale skeleton also increased the amount of time they spent swimming [19].”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [19] Larsson, A. (2012). Development and Evaluation of Environmental Enrichment for Captive Humboldt penguins, Swedish University of Agricultural Sciences.

      Not checked in the free run.

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

    Interpretationreasoning

    The increased walking during the breeding season likely reflected species-typical behaviors related to mate and breeding site selection.

    “The increased walking during the breeding season likely reflected species-typical behaviors related to mate and breeding site selection.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Interpretationown data

    Feeding practices were consistent between habitats in this study and likely do not explain the increased amount of time spent swimming in the PPCC.

    “Regardless, feeding practices were consistent between habitats in this study and likely do not explain the increased amount of time spent swimming in the PPCC.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Interpretationreasoning

    Lola's behavior shows how individual differences in age and health can impact behavioral choices, highlighting the importance of assessing welfare at the individual level.

    “Lola’s behavior shows how individual differences in age and health can impact behavioral choices, highlighting the importance of assessing welfare at the individual level.”
    Quote in the paperNot a substantial claim
    • Rests on an assumption: Welfare is experienced at the individual level.

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

    Premisereasoning

    It can be difficult, if not impossible, to identify specific causal factors for changes in animal behavior in most POE studies, given the multitude of factors that are generally altered in habitat improvements and the entangled relationship between space and complexity.

    “As these examples illustrate, it can be difficult, if not impossible, to identify specific causal factors for changes in animal behavior in most POE studies, given the multitude of factors that are generally altered in habitat improvements and the entangled relationship between space and complexity.”
    Quote in the paperNot a substantial claim

  • Classified as probably not a substantial claim.

    Study design and conductnone given

    One strength of this study was the ability to track penguins on an individual basis.

    “One strength of this study was our ability to track penguins on an individual basis.”
    Quote in the paperSubstantial claim

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

    Premisecitation

    Pool use by a group of gentoo penguins was correlated with higher visitor numbers, as was the overall behavioral diversity expressed by the penguin group.

    “Finally, pool use by a group of gentoo penguins (Pygoscelis papua) was correlated with higher visitor numbers, as was the overall behavioral diversity expressed by the penguin group [20].”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [20] Collins, 2016, The effect of the zoo setting on the behavioural diversity of captive gentoo penguins and the implications for their educational potential, J. Zoo Aquar. Res. source

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

    Study design and conductnone given

    None of the variables (either outcome or predictors) were multicollinear.

    “Before beginning advanced inferential statistics, we confirmed that none of the variables (either outcome or predictors) were multicollinear.”
    Quote in the paperNot a substantial claim

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

    Premisecitation

    Macaroni and southern rockhopper penguins increased their time spent swimming, as well as their overall habitat use, after receiving phacoemulsification surgery for cataract removal.

    “Using pressure sensors (time–depth recorders; TDRs), another study found that macaroni (Eudyptes chrysolophus) and southern rockhopper (E. chrysocome) penguins increased their time spent swimming, as well as their overall habitat use, after receiving phacoemulsification surgery for cataract removal [23].”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [23] Heintz, 2019, Case studies of the impacts of cataract surgery on crested penguin welfare, J. Appl. Anim. Welf. Sci. source

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

    Study design and conductown data

    The consistency in trends across phases as established by the Wilcoxon tests did not necessitate the inclusion of "phase" as a predictor variable in all GLMMs.

    “Although data were collected in two distinct phases (see Table 1), the consistency in trends across phases as established by the Wilcoxon tests did not necessitate the inclusion of “phase” as a predictor variable in all GLMMs.”
    Quote in the paperNot a substantial claim

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

    Premisecitation

    Hatching success for Humboldt penguins increased with greater pool size in a survey of British zoos.

    “hatching success for Humboldt penguins increased with greater pool size in a survey of British zoos [22].”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [22] Blay, 2001, Optimal conditions for breeding of captive Humboldt penguins (Spheniscus humboldti): A survey of British zoos, Zoo Biol. source

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

    Study design and conductnone given

    Penguin management was relatively consistent throughout the study.

    “Penguin management was relatively consistent throughout the study.”
    Quote in the paperNot a substantial claim

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

    Study design and conductnone given

    Observers recorded data on the penguins in the order they were listed to avoid any selection bias for observing birds more readily visible or engaged in more conspicuous behaviors.

    “Observers recorded data on the penguins in the order they were listed to avoid any selection bias for observing birds more readily visible or engaged in more conspicuous behaviors.”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S1 (asserted).

    Study design and conductown data

    The study used GLMMs to confirm that other confounding variables were not better predictors of differences in observed behavior.

    “Although habitat was our primary predictor variable of interest, we wanted to confirm that other confounding variables were not better predictors of differences in observed behavior. As such, we elected to run generalized linear mixed models (GLMMs) on counts of behaviors using the GLIMMIX procedure.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Study design and conductnone given

    The temperature of the PPCC pool is colder than that of the Penguinarium, and temperature differences between the habitats cannot be ruled out as a factor shaping the penguins' preference.

    “The temperature of the PPCC pool is colder than that of the Penguinarium, and we cannot rule out the temperature differences between the habitats as a factor shaping their preference.”
    Quote in the paperNot a substantial claim

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

    Study design and conductown data

    These behaviors were both fairly rare, and it is difficult to determine whether these trends were due to differences in the composition of study subjects or another factor.

    “These behaviors were both fairly rare, and it is difficult to determine whether these trends were due to differences in the composition of study subjects or another factor.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Interpretationown data

    The penguins shifted their activity from land to water by decreasing their time spent walking and spending more time swimming.

    “Instead of increasing their overall activity levels, the penguins shifted their activity from land to water by decreasing their time spent walking and spending more time swimming.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Interpretationreasoning

    Although ice did not appear to increase agonism in this study, together these findings indicate that ice is a highly preferred resource for king penguins.

    “Although ice did not appear to increase agonism in this study, together these findings indicate that ice is a highly preferred resource for king penguins.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Interpretationreasoning

    Given the differences in subjects and data collected between the two phases, we cannot definitively say that snow caused the increased laying, but it seems likely.

    “Given the differences in subjects and data collected between the two phases, we cannot definitively say that snow caused the increased laying, but it seems likely.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Study design and conductreasoning

    Because the PPCC is both substantially larger and more complex than the Penguinarium, it is still not possible to tease apart the relative contributions of habitat size and complexity.

    “Yet, because the PPCC is both substantially larger and more complex than the Penguinarium, it is still not possible to tease apart the relative contributions of habitat size and complexity.”
    Quote in the paperSubstantial claim

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

    Interpretationreasoning

    A multi-institutional study design is likely needed to determine how space and complexity differentially affect animal welfare.

    “A multi-institutional study design is likely needed to determine how space and complexity differentially affect animal welfare.”
    Quote in the paperNot a substantial claim

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

    Interpretationreasoning

    Incorporating preferred features into habitat design is likely to generate the greatest benefits for animal welfare.

    “Thus, incorporating preferred features into habitat design is likely to generate the greatest benefits for animal welfare [55].”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [55] Ross, 2009, Space use as an indicator of enclosure appropriateness: A novel measure of captive animal welfare, Appl. Anim. Behav. Sci. source

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

    Interpretationnone given

    Although a POE for one group cannot identify species trends, welfare is experienced at the individual level, and a POE can say a lot about what individual animals want.

    “Although a POE for one group cannot identify species trends, welfare is experienced at the individual level, and a POE can say a lot about what individual animals want.”
    Quote in the paperNot a substantial claim
    • Rests on an assumption: Welfare is experienced at the individual level.

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

    Interpretationreasoning

    Giving animals what they want depends on conducting studies like these across varied contexts in order to establish ideal habitat design and management processes.

    “However, giving animals what they want depends on conducting studies like these across varied contexts in order to establish ideal habitat design and management processes.”
    Quote in the paperNot a substantial claim

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

    Study design and conductown data

    One of the limitations of this study is that we did not identify the individuals to whom focal penguins were in proximity, so we cannot comment on how their social networks or pair bonds could have affected proximity patterns.

    “One of the limitations of this study is that we did not identify the individuals to whom focal penguins were in proximity, so we cannot comment on how their social networks or pair bonds could have affected proximity patterns.”
    Quote in the paperNot a substantial claim

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

    Interpretationcitation

    By Dawkins's definition, giving animals what they want should improve their welfare.

    “By Dawkins’s definition, giving animals what they want should improve their welfare.”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [54] Dawkins, M.S. (2021). The Science of Animal Welfare: Understanding What Animals Want, Oxford University Press. source
78 of 78

  • The paper relies on this without support.

    The behavioral changes observed (increased swimming, decreased aggression, increased positive social behaviors, etc.) are valid indicators of positive welfare for king penguins.

    “Using the behavioral observations, we identified a subset of interval, all-occurrence, and proximity behaviors of interest as potential welfare indicators.”
    “These behavioral trends suggest that increased space and environmental complexity had positive welfare benefits for these penguins.”

  • The paper relies on this without support.

    The differences in behavior between the Penguinarium and PPCC are attributable to the increased space and environmental complexity of the PPCC, rather than to other differences between the habitats.

    “As these examples illustrate, it can be difficult, if not impossible, to identify specific causal factors for changes in animal behavior in most POE studies, given the multitude of factors that are generally altered in habitat improvements and the entangled relationship between space and complexity.”
    “These behavioral trends suggest that increased space and environmental complexity had positive welfare benefits for these penguins.”

  • The paper relies on this without support.

    The behavioral changes observed (e.g., increased swimming, increased positive social behavior, decreased agonism) are valid indicators of improved welfare.

    “Overall, the king penguins in this study demonstrated increases in positive welfare indicators when they occupied the PPCC compared to the Penguinarium, although these changes did not follow the exact patterns we predicted.”
    “Ultimately, moving to the larger, more complex PPCC appeared to have positive benefits for the welfare of these king penguins.”

  • The paper relies on this without support.

    Welfare is experienced at the individual level.

    “Although a POE for one group cannot identify species trends, welfare is experienced at the individual level, and a POE can say a lot about what individual animals want.”
4 of 4

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.

  • Opposite sex differences in display rate

    Major

    The results describe display rates as higher among females, while the discussion says males displayed more than females.

  • Direction of proximity to other king penguins reverses

    Major

    The results say the penguins spent more time near other king penguins in the PPCC, but the discussion says they spent less time near conspecifics there.

  • Opposite breeding-season effects on displays

    Major

    The results describe display rates as higher in the breeding season, while the discussion says the mixed model found fewer displays during that season than during the nonbreeding season.

  • Bathing is reported as higher in opposite habitats

    Major

    The phase-by-phase results say bathing rates were higher in the Penguinarium in both phases, while the aquatic-behavior results say they were significantly higher in the PPCC.

  • Age both does and does not influence proximity

    Minor

    The results say age significantly influenced proximity patterns, but the discussion says the mixed model identified no demographic factor such as age that explained them.

5 of 5

Cites

Flagged first, then by citations

Research works printed but not linked: 1

  1. Waterfall, K., Kottyan, J., Sirpenski, G., Huetnner, S., and Schneider, T. (2020). AZA Penguin Regional Collection Plan 2020–2025, Association of Zoos and Aquariums.

Cited by

Sorted by citations

Related

Authors
Fuller, G., Jones, M., Gartland, K. N., Zalewski, S., Heintz, M. R., & Allard, S.
Affiliations
  • Center for Zoo and Aquarium Animal Welfare and Ethics, Detroit Zoological Society, Royal Oak, MI 48067, USA
  • National Aquarium (US)
Corresponding author
Fuller, Grace
ORCID
Venue
Animals
Publisher
MDPI AG
Published
2023-07-14
Volume
13
Issue
14
Pages
2312
ISSN
2076-2615 (ISSN-L)
DOI
10.3390/ani13142312
PMC
PMC10376525
OpenAlex
W4384525651
Semantic Scholar
4497566c310c120a4f1bbc7877c2442e447eb2ca
Cited by
8
References
50
Citations by year
2026: 3 · 2025: 2 · 2024: 2 · 2023: 1
FWCI
2.12
Type
journal article
Language
en
Open access
Licence
Locations
  • Animals (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • PubMed Central (submittedVersion, cc-by)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Topics
  • Health Sciences › Veterinary › Small Animals › Animal Behavior and Welfare Studies
  • Physical Sciences › Environmental Science › Ecology › Avian ecology and behavior
  • Physical Sciences › Environmental Science › Ecology › Marine animal studies overview
Keywords
king penguin, Aptenodytes patagonicus, animal welfare, habitat complexity, space use, penguin behavior, aggression, swimming behavior, social behavior, time-depth recorders

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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