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Thank you for carrying out further revisions to the manuscript. I believe that the review has benefited substantially from the robust discussions that have taken place as part of the review process.
[# PeerJ Staff Note - this decision was reviewed and approved by Jennifer Vonk, a PeerJ Section Editor covering this Section #]
As you can see from the reviewer comments, this manuscript has generated very opposing views. Two reviewers are largely happy with the structure and contents of the review, while two others are not. I am prepared to allow one more, final round of careful revisions that hopefully can strike some balance between the opposing views. Given the comments, it seems unlikely that a consensus will be reached.
It is also worth noting that PeerJ policy is that additional references suggested during the peer-review process should only be included if the authors agree that they are relevant and useful.
**PeerJ Staff Note**: Please ensure that all review, editorial, and staff comments are addressed in a response letter and that any edits or clarifications mentioned in the letter are also inserted into the revised manuscript where appropriate.
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In general, I am satisfied with the revisions the author has made.
I just have a couple of minor comments: the author uses the term “anthropocentric noise,” but I believe they intended to say “anthropogenic noise.”
Additionally, I was expecting the requested summaries to be included in the Discussion section. This is typically where readers benefit from a brief recap of the previous sections, especially as those results are being interpreted and contextualized there.
Regarding your response to line 71, I am surprised there is no reference to a decree or official document number, assuming these were decisions made by the authorities.
No more comment
No more comment
As a review paper, despite its heavy revisions, it still fails at its two ultimate goals of A) convincing the reader that, as a population, animals under managed care are experiencing uniformly poorer welfare than their wild counterparts, B) that the welfare of cetaceans in zoos and aquariums would be uniformly improved by movement into GFAS accredited sanctuaries. I fear no amount of revision can make this article successful in these endeavors. As an exercise, the authors should consider attempting to make the argument that cetaceans experience, poorer welfare in zoos and aquariums without widespread self-citation, misrepresentation of other authors, or omission from other authors. Taking Marino et al.,'s referencing of my own paper as an example, Marino et al., misleadingly implies that Bruck, 2024 believes the challenges associated with feeding, veterinary care and funding are shared equally by GFAS sanctuaries and Alliance accredited marine mammal facilitates. The entire thrust of that paper highlights why those issues are exacerbated by the prescriptions of GFAS accreditation. There are issues like this throughout that render the paper unfit for publication under any pretense that these are neutral observers just calling balls and strikes. If this were a an opinion commentary or philosophy paper in another journal I would be less inclined to protest; however, these authors are attempting to pass this off as a neutral and even handed evaluation of the current state of captivity for cetaceans and after reading both its original version and now this revised one I can't help but get the impression that none of these authors have set foot or much less worked with a modern accredited zoo or aquarium or their animals. Furthermore, there is a serious lack of data supporting the position that the population of animals in zoos and aquariums are in dire need of intervention and that that intervention should be sea pen sanctuaries. The authors expressed some disagreements with the cetacean welfare study's methodology but offer no competing data of their own that improves on those perceived limitations (which I explain below do not actually undercut the main theses of those papers). Surely if the animals are experiencing uniformly, poor welfare there should be a convincing case in the literature. These animals represent significant investments for the facilities that house them. One should expect at least some literature examining those issues. Rather, these authors have built a house of publications criticizing the welfare of animals in zoos and aquariums, without a foundation of data to support their conclusions. This has led to a perpetual ring of self-citations with the goal of achieving a false consensus to their conclusions. Meanwhile sleight of hand is used to both emphasize the scientific immeasurability of "quality of life" only to imply that the animals in zoos either have a poor quality of life or would have their quality of life improved by living in a GFAS sanctuary. Meanwhile no data are present to support those conclusions because quality of life is subjective and even if you could base it on good welfare data, the authors do not present any of it to at least imply that GFAS sanctuaries would lead to at least something most cetacean welfare experts might subjectively assess to be a "quality of life" improvement. In this case the authors should identify any data they can manage from the Beluga Sea Life Sanctuary that might explain why, after 5+ years of living in a pool instead of their sea pen, Little Grey and Little White would still benefit from living in that sea pen sanctuary, despite multiple attempts to put them out there and multiple trips back to the pool. Perhaps there is a C-Well assessment that shows, despite all appearances, the belugas did have better welfare in the sea pen than the pool, and that would be a great thing to have in a paper ostensibly about the current state of captive cetacean welfare. Do the authors know how well the animals were stationing in the sanctuary? Or if they showed any signs of stress in the sanctuary like ulcers for example? Those would be good things to discuss with readers, if this paper is about the current state of captivity and why it is bad and these animals need to be in sanctuaries. While I cast no aspersions on the authors, such data would also go a long way toward showing that the lead author who happens to be president of the Whale Sanctuary Project (and, to my knowledge, still draws salary from that) is fully aware of the issues she may confront when housing her own animals in the way she elected to when writing the GFAS standards.
As far as my review, again I have chosen to directly edit the manuscript and put comments upon it as they are extensive. New comments have my name on them (old comments that weren't addressed satisfactorily or are needed for context remain with the name 'author' on them). Some of the author responses to my comments are replied to here, however, for the sake of time, I have chosen to respond to only those comments that I think the authors struggled most with or would lead to some improvement.
That being said, I must again offer that this is not the format or journal for this work. The authors do not have sufficient data, nor do they reference studies with sufficient data to make the points they are making convincingly. Much of this is opinion, and not fact. If this were to be published, I would recommend focusing not on speculation, but what is not known about cetacean welfare in zoos and how we could get at those questions honestly. To do this and to provide more captive cetacean experience to the paper, the authors should seriously consider adding an additional author or two who does not share blanket anti-captivity views to help balance out the paper. I would recommend finding a current zoo professional (someone like Lance Miller or Jessica Whitham) who works with animals/welfare and a welfare specialist (like Fabienne Delfour or Kathleen Dudzinski) to round out the author list and provide deeply needed perspective.
I maintain many of the same issues are present from before. I haver highlighted issues in the manuscript itself along with responses to the reviewer responses.
I maintain many of the same issues are present from before. I haver highlighted issues in the manuscript itself along with responses to the reviewer responses.
Again, I applaud the authors’ stated intention to provide “an accurate, comprehensive and current picture of the status of captive cetaceans” [L. 174]. This is a laudable goal that falls within the scope of this journal. Unfortunately, however, the current manuscript still falls dramatically short of this goal in quite a few ways, including in some new ways. (See below)
Also, in my previous comments, I noted that this review is similar in substance to two other reviews by some of the same authors in recent years, with largely the same arguments and conclusions.
• Jacobs, B., Rally, H., Doyle, C., O’Brien, L., Tennison, M., & Marino, L. (2022). Putative neural consequences of captivity for elephants and cetaceans. Reviews in the Neurosciences, 33(4), 439–465. https://doi.org/10.1515/revneuro-2021-0100
• Marino, L., Rose, N. A., Visser, I. N., Rally, H., Ferdowsian, H., & Slootsky, V. (2020). The harmful effects of captivity and chronic stress on the well-being of orcas (Orcinus orca). Journal of Veterinary Behavior, 35, 69–82. https://doi.org/10.1016/j.jveb.2019.05.005
To that I would add a third, more recent review of theirs that also discusses these same issues:
• Marino, L., Doyle, C., Rally, H., O'Brien, L., & Jacobs, B. (2025). Captive elephants and cetaceans: The misery of the menagerie. Metode Science Studies Journal, 15(5), e29118-e29118.
The current manuscript still does not give an accurate review of the scientific literature on this topic. The authors did make a number of changes suggested by reviewers. However, there are still numerous instances (including new instances) where: (a) the references cited do not support the data or claims attributed to them; (b) directly relevant references that should be cited are omitted from the discussion; and/or (c) supporting evidence is presented from a cited reference, while potentially opposing evidence from that same reference is omitted. For example:
L 212-213 states: “There is considerable variation in tank size across facilities. Many tanks are too small or shallow to allow natural swimming behaviors (Corkeron, 2009; Lott & Williamson, 2017).”
• In the previous manuscript, McPhee & Carlstead, 2010 were referenced for this claim. I commented that McPhee & Carlstead, 2010, doesn’t say this, to which the authors replied that I was correct, and that they had replaced the reference. However, of the new references for this claim: The Corkeron article also does not say what is being attributed to it. What it actually says is that this is the argument that is made by people who are opposed to cetaceans in captivity. The Lott & Williamson article simply notes that facility enclosures are not nearly as large as the space naturally available in the wild, and that the animals therefore need to swim in circles rather than a straight line to travel the same distance as their wild counterparts.
L 310-311 states: “Moreover, any sharp angles in a tank can cause potentially stressful reverberations (Wright et al., 2007; Huettner et al., 2021).”
• Neither of these articles talks about angles in a tank, as is claimed here. (In fact, if I remember correctly, the dolphins in the Huettner study were housed in lagoons that mimicked a natural lagoon, without sharp angles.)
L 365. The Clegg et al (2023) paper didn’t report any data on logging.
L 426-428 states: “There is some evidence to suggest that positive reinforcement training can help to decrease stereotypic behavior and the stress of husbandry and medical procedures in other species in captivity (Desportes et al., 2007; Coleman & Maier, 2010)”
• Please note that the Desportes et al article cited here is in fact about cetaceans in facilities, and not "other species."
• In addition, the authors are understating the positive welfare effects that have been found from positive reinforcement training – which have included increasing activity levels, behavioral variability, and habitat utilization, as well as decreasing aggression, stereotypies, and other stress-related behaviors. Please see, e.g.,
o Bassett, L. et. al (2003). Effects of training on stress-related behavior of the common marmoset (Callithrix jacchus) in relation to coping with routine husbandry procedures. Journal of Applied Animal Welfare Science, 6, 221-233.
o Grant, R. A., & Warrior, J. R. (2019). Clicker training increases exploratory behaviour and time spent at the front of the enclosure in shelter cats: Implications for welfare and adoption rates. Applied Animal Behaviour Science, 211, 77–83.
o Kastelein, R. A., & Wiepkema, P. R. (1988). The significance of training for the behaviour of Steller sea lions (Eumetopias jubata) in human care. Aquatic Mammals, 14(1), 39-41.
o Pomerantz, O., Terkel, J., 2009. Effects of positive reinforcement training techniques on the psychological welfare of zoo-housed chimpanzees (Pan troglodytes). Am. J. Primatol. 71 (8), 687–695.
o Shyne A and Block M 2010 The effects of husbandry training on stereotypic pacing in captive African wild dogs (Lycaon pictus). Journal of Applied Animal Welfare Science 13: 56-65.
**PeerJ Staff Note:** It is PeerJ policy that additional references suggested during the peer-review process should only be included if the authors are in agreement that they are relevant and useful.
L 428-433 states: “however, it is unclear how and when various forms of training correlate with overall enhanced enrichment and well-being for captive wildlife (Melfi, 2013; Fernandez, 2022). Thus, it is clear that more research is required to understand which components of training and performance are indeed enriching rather than just providing temporary relief from boredom, creating a distraction, or otherwise occupying the time budget of captive cetaceans.”
• This presents a misleading interpretation of the cited literature. In particular, Fernandez (2022) concludes that existing evidence supports the role of training in enhancing enrichment usage, modifying animal–human interactions, and expanding behavioral repertoires in ways that benefit animal welfare. While the author does note the need for continued research, this is in the context of “expanding our understanding of the conditions under which training might function as enrichment”—not questioning the fundamental potential of training to serve as enrichment.
• In addition, given that these studies specifically examine welfare outcomes that extend beyond the duration of training sessions, the effects indicated are in fact inconsistent with mere temporary distraction or time-budget occupation.
L 531 states: “Also found in captive cetaceans are circling and repetitive swimming patterns (Jett & Ventre, 2011; Ugaz et al., 2013).”
• The Jett & Ventre white paper cited here does not present data on, or even discuss, circling and repetitive swimming patterns.
L 576-578 states: “captive bottlenose dolphins and other cetaceans, especially those in interaction and feeding sessions with the public and SWD programs, also have a long record of aggression towards humans, often resulting in severe human injuries (Anderson et al., 2016).”
• The reference cited does not say what is claimed here. Anderson et al. (2016) is about orcas, not bottlenose dolphins, and none of the animals had been in Swim-With-Dolphin (SWD) programs. Moreover, for the two standout orcas with the highest number of reported incidents, one had been in the petting pool as a young juvenile (12 incidents) and one had not (17 incidents). There were no statistical differences between groups.
• Additionally, in the previous version of this manuscript, the authors cited Shane et al. (1993) and Spradlin et al. (1999) for this same assertion. In response to my comments that those articles concern interactions with wild cetaceans, not captive ones, those citations appear to have simply been removed, without addressing the underlying misclassification of the source material. Notably, just a few lines earlier in the manuscript, the authors suggest that aggressive behavior by wild cetaceans toward humans is almost nonexistent. Therefore, I would suggest that those deleted references are in fact relevant to the discussion, and should be cited as such.
L 759-761 states. “Although more data are needed, captive cetaceans continue to experience an equivalent or higher risk of dying compared to conspecifics from healthy, free-living populations (Montano, 2017; Jaakkola & Willis, 2019; Rose et al., 2023).”
This statement is not supported by the cited references:
o Montano (2017) discusses the maximum lifespan of beluga whales, which is not equivalent to “risk of dying”.
o Jaakkola & Willis (2019) in fact report that recent survival rates for bottlenose dolphins in captivity are numerically higher than those of all three wild populations for which comparable data are available—two of which show statistically significant differences in favor of the captive population. This finding directly contradicts the claim made in the manuscript.
o Rose et al. (2023) is a non–peer-reviewed white paper that does not include data of its own, and that references a blog post summarizing a short undergraduate project—an unreliable and inappropriate source for supporting scientific conclusions. (Notably, the current authors removed their own reference to this blog post from the manuscript in response to previous reviewer feedback.)
Furthermore, as noted in my earlier review, Tidière et al. (2023) found that the life expectancy of captive bottlenose dolphins has been significantly higher than that of wild dolphins for several decades. Although the authors cite this paper in a later section, they omit this key finding, which directly contradicts the claim made here.
L 770-772 states: “One recent study suggested that mean life expectancy for captive bottlenose dolphins is not significantly different from that in some free-living populations (Jaakkola & Willis; 2019).”
• As noted above and in my previous review, this is misleading. Jaakkola & Willis (2019) in fact report that recent survival rates (and therefore life expectancies) for bottlenose dolphins in captivity are numerically higher than those of all three wild populations for which comparable data are available—two of which show statistically significant differences in favor of the captive population.
L 772-773 states: “The most recent study of longevity also indicates improvements in life expectancy and first year survival rates for captive bottlenose dolphins (Tidière et al., 2023).
• I appreciate the authors’ inclusion of this important and relevant reference. However, the manuscript still omits one of the most critical findings from Tidière et al. (2023)—a point I raised in my previous review. Specifically, the study found that for the past several decades, the life expectancy of captive bottlenose dolphins has been significantly higher than that of their wild counterparts. This result is directly relevant to the manuscript’s discussion of welfare and survival and should be clearly acknowledged in this section.
L 767 notes that Wells et al. (2013) suggest an average age at death of 19.9 years for one population of wild bottlenose dolphins. This value is accurately reported, however, the authors have omitted a key contextual statement from Wells et al. (2013) that is directly relevant to the discussion of life expectancy. In the same paragraph from which the 19.9-year figure is drawn, the authors state: “Comparisons of age at death with Sarasota Bay dolphins suggest that the managed population studied by Venn-Watson et al. (3) is indeed older.” I recommend including this information to ensure a more complete and accurate representation of the cited source and to enhance the manuscript’s discussion of comparative longevity.
L 783-792 re: Life expectancy in orcas -- The issue of life expectancy in captive versus wild orcas has been the subject of a well-documented and ongoing scientific debate, as highlighted in Callaway (2016). The two principal data papers in this area—Robeck et al. (2015) and Jett & Ventre (2015)—present differing conclusions. Each was followed by subsequent peer-reviewed commentary (e.g., Franks et al., 2016; Robeck et al., 2016; Jett, 2016).
In my previous review, I noted that the manuscript omitted any discussion of this extensive literature, especially the two foundational data papers. The authors have since agreed to cite the Jett & Ventre paper, whose conclusions align with their narrative. However, they declined to cite the Robeck et al. paper (whose data contradicts their argument), claiming that it is “flawed in this regard”, for which they appeal to a footnote in a non-peer-reviewed white paper as justification. I would suggest that this is an unacceptable way to handle a scientific controversy within a review paper about this topic.
A balanced and responsible literature review should present both sides of this well-known scientific controversy. Selectively citing only one perspective undermines the credibility of the review.
References:
• Callaway, E. (2016). Scientists clash over lifespan of captive killer whales. Nature, 531(7595), 426–427. https://doi.org/10.1038/531426a
• Jett, J., & Ventre, J. (2015). Captive killer whale (Orcinus orca) survival. Marine Mammal Science, 31(4), 1362–1377. https://doi.org/10.1111/mms.12225
• Robeck, T. R., Willis, K., Scarpuzzi, M. R., & O’Brien, J. K. (2015). Comparisons of life-history parameters between free-ranging and captive killer whale (Orcinus orca) populations for application toward species management. Journal of Mammalogy, 96(5), 1055–1070. https://doi.org/10.1093/jmammal/gyv113
• Franks, D. W., Nattrass, S., Brent, L. J. N., Whitehead, H., Foote, A. D., Mazzi, S., Ford, J. K. B., Balcomb, K. C., Cant, M. A., & Croft, D. P. (2016). The significance of postreproductive lifespans in killer whales: A comment on Robeck et al.: Table 1. Journal of Mammalogy, 97(3), 906–909. https://doi.org/10.1093/jmammal/gyw021
• Robeck, T. R., Willis, K., Scarpuzzi, M. R., & O’Brien, J. K. (2016). Survivorship pattern inaccuracies and inappropriate anthropomorphism in scholarly pursuits of killer whale (Orcinus orca) life history: A response to Franks et al. (2016). Journal of Mammalogy, 97(3), 899–905. https://doi.org/10.1093/jmammal/gyw023
• Robeck, T., Jaakkola, K., Stafford, G., & Willis, K. (2016). Scientific Correspondence: Killer whale (Orcinus orca) survivorship in captivity: A critique of Jett and Ventre (2015). Marine Mammal Science, 32(2), 786–792. https://doi.org/10.1111/mms.12278
• Jett, J. (2016). Scientific Correspondence: Response to Robeck et al .’s critique of Jett and Ventre (2015) captive killer whale (Orcinus orca) survival. Marine Mammal Science, 32(2), 793–798. https://doi.org/10.1111/mms.12313
L 794-5 states: “For free-living beluga whales, mean life expectancy is ~20-30 years and maximum ~60 years (Lockyer et al., 2007; Wells & Scott, 2009; Willis, 2012).”
• The references cited here do not contain the information attributed to them.
o Lockyer et al. (2007) does not provide estimates of mean life expectancy or maximum age for free-ranging belugas.
o Wells & Scott (2009) is focused on bottlenose dolphins and does not include any data or discussion pertaining to beluga whales.
o The Willis (2012) white paper notes that the mean life expectancy calculated from different studies has an extremely large range (from ~12-66 years) “likely due to several factors including differences among the studied populations, sampling methodology (harvested versus stranded beluga), and the statistical methodologies used to derive the estimates.” It does not provide an estimate of maximum lifespan for free-ranging belugas.
L 797-798 states: “The best estimation for maximum longevity in captive beluga whales is 35 years of age (Montano et al., 2017).”
• While this citation correctly reflects the estimate for captive beluga whales reported in Montano et al. (2017), the authors omit closely related and highly relevant comparative data provided in the same section of that reference. – i.e., “Studies performed on development and growth of the beluga in the wild suggest a maximum lifespan of 32 years (Sergeant 1959), 40 years (Khuzin 1961 as cited by Brodie 1971), 20–32 years (Kleinenberg et al. [1964] 1969) and 30 years (Brodie 1969, as cited by Brodie 1971). A recent review on beluga age estimation based on markers within teeth supports a maximum longevity of 30–35 years in free-ranging animals (Brodie et al. 2013).” This context is essential for a meaningful interpretation of the reported captive longevity figure, and should be included.
There are a number of misleading arguments throughout the manuscript, including:
L 216-219 states: “under the federal Animal Welfare Act (2025), which is enforced by the United States Department of Agriculture, the minimum size standard for orca enclosures is 15 m for minimum horizontal distance (i.e., length and width) and 4 m for minimum depth, which severely limits natural movements, postures, and behaviors”
• Measurements of minimum legal space are not the same as measurements of the space in which the animals are actually housed. The relevant data for assessing welfare must be how the animals are actually housed, as this is the factor that could impact the animals. Are there any orcas in U.S. facilities that are currently housed in enclosures of this size? If such cases exist, they should be cited with appropriate references. If not, then the inclusion of these dimensions is misleading, as it implies a welfare limitation that does not reflect the real conditions experienced by the animals in question.
L 269-280. The authors argue that the minimal differences in welfare outcomes across enclosure sizes may be due to a floor effect, suggesting that the limited range of enclosure sizes in current research, which are of course smaller than the animals’ natural habitats, might prevent meaningful effects from emerging. While such a hypothesis is possible in theory, it is also at this point entirely speculative, and should not be used to discount actual empirical findings.
The reality is that the minimal differences in welfare outcomes across enclosure sizes could theoretically be due to several possibilities, all of which deserve equal consideration. Specifically:
1. The findings may accurately reflect that enclosure size is not a primary driver of welfare outcomes for cetaceans in marine mammal facilities.
2. A floor effect could exist, such that larger enclosures than those currently studied might yield detectable differences.
3. Conversely, a ceiling effect may exist, whereby welfare deficits are evident only in unusually small enclosures, with more standard sizes already sufficient to mitigate those effects.
Importantly, there is empirical support for this third interpretation. Dolphins in undersized enclosures have exhibited elevated aggression and stereotypic behaviors such as head-pressing, both of which disappeared after relocation to more typical-sized enclosures (Greenwood, 1977; Myers & Overstrom, 1978).
L 400-418 re: Animal Welfare Act (2025) standards – This entire section is incorrect and misleading. The standards referenced here as part of the Animal Welfare Act (AWA) were suspended more than 25 years ago, as is explicitly stated on the same USDA webpage the authors cite as their source: “Effective Date Note: At 64 FR 15920, Apr. 2, 1999, § 3.111 was suspended, effective Apr. 2, 1999.” As such, these are not current legal standards and should not be represented as such.
L 456-459 states: “Therefore, although there are reasons to view interactions with humans – and in particular the public – as negative for captive dolphins, it is yet to be determined which specific components of those activities (and those before or after) are important factors in how dolphins react.”
• This conclusion misrepresents the evidence presented in the manuscript. Specifically, the studies cited show a pattern in which interactions with trainers—typically involving structured, staff-mediated swim programs—are associated with potentially positive welfare outcomes, while unstructured swim programs were linked to more ambiguous or negative effects. (Note that Kyngdon et al., 2003, was an unstructured swim situation, although it wasn’t presented as such). Given this pattern, a more accurate and evidence-based interpretation would be to state that while some evidence suggests unstructured swim programs may be associated with negative responses, structured, trainer-mediated interactions seem to have positive effects on welfare.”
L 490-492 states: “Despite decades of housing cetaceans in captivity and efforts by accredited zoos and aquaria to modify their facilities, husbandry, and preventative medical programs to reduce these diseases, many of them persist.”
• This is an odd argument at best. The survival rates and life expectancies of cetaceans in facilities have increased dramatically over the last several decades (Jaakkola & Wills, 2019; Jett & Ventre, 2015; Robeck et al., 2015; Tidière et al., 2023) Are the authors suggesting that there should be no disease because there is health care? Clearly this would be an unrealistic standard. Are there any human populations for which this is true?
L 508-510 states: “The chronic stress of coping with the various dimensions of captivity over time has an impact on mental and physical health in cetaceans, as it does in every other species (Marino et al., 2020).”
• The fact that chronic stress negatively affects physical and mental health across species is indeed well-established. However, the key empirical question here is whether the conditions of captivity are, in fact, chronically stressful for cetaceans. This distinction is critical, and cannot simply be assumed or stipulated. The claim made in this sentence appears to conflate these two issues, treating the presence of chronic stress in captivity as a given without providing supporting empirical evidence. This assertion relies on Marino et al. (2020)—a prior review by the same authors—which similarly presupposed chronic stress. However, note that other peer-reviewed literature has challenged this assumption (e.g., Dudzinski et al., 2020; Jaakkola et al., 2020).
o Dudzinski, K. M., Hill, H. M., Zaccaroni, A., Makecha, R., Lilley, M., Almunia, J., Frick, E., Feucht, T., Stafford, G., & Abramson, C. I. (2020). Distinguishing personal belief from scientific knowledge for the betterment of killer whale welfare – a commentary. International Journal of Comparative Psychology, 33. https://doi.org/10.46867/ijcp.2020.33.00.01
o Jaakkola, K., Bruck, J. N., Connor, R. C., Montgomery, S. H., & King, S. L. (2020). Bias and Misrepresentation of Science Undermines Productive Discourse on Animal Welfare Policy: A Case Study. Animals, 10(7), 1118. https://doi.org/10.3390/ani10071118
L 85-86 states: “In China, the captive cetacean entertainment industry has been growing precipitously over recent years (Ong, 2017).”
• What is meant by “precipitously” here? The reference cited only includes a single line stating that “The numbers of animals in captivity that are deployed for tourism performances are on the rise,” with no data are given to support this statement.
L87 states: “Globally, more than 3,500 cetaceans are housed in concrete tanks or small pens in ~350 marine parks, zoos, and military facilities (Cetabase, 2024).”
• How are the authors defining “small pens” here? The reference cited doesn’t talk about pen size at all.
L96 states: “Animals in zoos and marine parks in the U.S. are covered by minimal regulations set forth under the Animal Welfare Act”
• How are the authors defining “minimal regulations”, as opposed to just “regulations”?
L 176-177 states: “Finally, findings from secondary sources (e.g., review articles, online web pages) were confirmed in primary sources whenever possible.”
• It would be helpful to clarify under what circumstances confirmation from primary sources was not possible. In particular, I worry that this means that unconfirmed information from web pages (for example) could be included as a purportedly reliable source. To ensure the reliability of the information presented, it would be useful if the authors would explicitly state whether any unverified content from web pages or other secondary sources was included.
L 220–223 notes that one of the largest orca pools in the world is considerably smaller than the Salish Sea. While this is factually correct, it is also a generalizable observation that applies to all captive animals—zoological enclosures are necessarily smaller than the animals’ natural habitats. For example, the largest lion enclosure in captivity is vastly smaller than the Serengeti, yet this observation alone does not inform welfare assessments.
L 244-246. It would be relevant to note here that the vast majority of bottlenose dolphins in facilities come from the coastal ecotype.
L 257-260 states: “Cetacean Welfare Study, which found that dolphins in managed ocean habitats swam in the top third of the water column less often than dolphins in managed zoo/aquarium habitats, presumably because they were exploring the more natural ocean environment”
• It is worth noting that this is only one of the possible explanations. The authors of this paper also noted that because the ocean habitats were shallower than zoo/aquarium habitats, this result could have been due to the fact that “top third” was smaller in the ocean habitats. For example, if the dolphins tended to swim at 2 m from the surface, that would have been coded as top third in the average zoo/aquarium habitat, but middle third in the average ocean habitat.
L 287-288 states: “In captivity, sensory-perceptual experiences are largely determined by the physical features of enclosures, which are relatively limited and unchanging.”
• This assertion needs justification. As written, it seems akin to saying that a person’s sensory experiences in a home or school are largely determined by the physical features of the walls, rather than by what is within those walls (which is clearly not true). In the previous paragraph, the manuscript notes that environmental enrichment and training schedules were found to have a greater impact on welfare indicators than enclosure features. How is this reconciled with the current statement?
L 289–290 quotes Jaakkola (2024) as stating: “these animals live in highly predictable and structured environments.” As presented, this excerpt misrepresents the original sentence by omitting critical context. The full quote continues with important qualifiers that affect its interpretation. To maintain accuracy, either the full sentence should be quoted, or an ellipsis should be used to indicate that material has been omitted.
L 292–293 states: “Underwater windows, if present, may further decrease the opportunity for captive animals to find refuge from visitor gaze.”
• This phrasing appears to assume that visitor gaze is inherently aversive or detrimental to animal welfare. Is there empirical evidence supporting this assumption? In the context of a paragraph emphasizing the limitations of unchanging physical features, one might reasonably hypothesize the opposite—that variable stimuli such as visitors could provide a form of enrichment. The authors should either provide empirical support for their interpretation of this, or revise the statement to avoid unsupported assumptions.
L 311-313 states: “In this regard, it has been suggested that smooth tank surfaces may result in reverberations that lead to reduced rates of echolocation (Rose et al., 2023).”
• This suggestion appears to originate from a white paper that asserts this claim without providing supporting data. As this manuscript is meant to be a review of scientific evidence, I would expect it to be grounded in peer-reviewed evidence rather than unsubstantiated assertions. If there are empirical data supporting this point, please cite them explicitly. Otherwise, this statement is unwarranted and should be omitted.
L 341–343 states: “Clegg & Butterworth (2017) noted that social group composition in captive facilities is largely artificial and under the control of zoo management rather than the animals themselves.”
• This misrepresents the original source, which described social group composition as “somewhat artificial,” not “largely artificial,” due to control by zoo management. It may also be worth noting that such management of social groups is a standard practice for every animal under any type of human care, including sanctuaries, and is generally regarded as important for maintaining animal welfare by mitigating potential social incompatibilities.
L 348-350 states: “Because captive cetacean groups do not resemble the multi-generational, strongly bonded social groups in the wild, there may be long-standing repercussions for the psychosocial well-being of calves.”
• This appears to be a speculative assertion that is not currently supported by cited empirical evidence. If such evidence exists, it should be referenced explicitly. Otherwise, unsubstantiated speculation such as this is unwarranted in a balanced review paper.
L 350-354 states: “In captivity, because of the artificial nature of the environment and the fact that calves of a number of cetacean species held in captivity are often separated from their mothers at a young age, whales and dolphins cannot learn the skills important to survival or essential nursing skills necessary to care for their own young (Rose et al. 2009).”
• Again, this claim is drawn from a white paper that presents the assertion without providing supporting data. As this manuscript is meant to be a review of scientific evidence, I would expect it to be grounded in peer-reviewed evidence rather than unsubstantiated assertions. If there are empirical data supporting this point, please cite them explicitly. Otherwise, this statement is unwarranted and should be omitted.
L 355-357 states: “The limited space available to groups of captive cetaceans may also impact their ability to use dispersal to keep intra-group aggression to a minimum, but this possibility has not been systematically studied.”
• Given the manuscript’s stated goal of providing “an accurate, comprehensive, and current picture of the status of captive cetaceans,” this type of speculative statement biased to a particular side risks undermining that objective. For a more neutral, evidence-based tone, I recommend rephrasing the sentence to reflect the lack of empirical study without implying a particular outcome. For example:
o “Whether the limited space available to groups of captive cetaceans impacts their ability to use dispersal to manage intra-group aggression has not yet been systematically studied,” or
o “The limited space available to groups of captive cetaceans may or may not affect their ability to use dispersal to minimize intra-group aggression. This question has not yet been systematically investigated.”
Lines 380–382 state that the process of eating food handed to captive cetaceans requires little to no cognitive effort on their part. However, the authors appear to have overlooked the cognitive effort involved in the training sessions through which food is typically delivered in marine mammal facilities. Even in the Clegg enrichment study that the authors praised earlier (Lines 253–256), the cognitive challenge occurred during the task preceding food delivery, not during consumption itself. Similarly, learning and doing behaviors during positive reinforcement training sessions requires cognitive effort and has been shown to have welfare benefits (Jaakkola, 2024). The authors should include consideration of the cognitive demands and potential welfare benefits associated with training-based feeding practices here to provide a more accurate assessment.
•Jaakkola, K. (2024). Minding the Minds: A Primer on Cognitive Challenge for Marine Mammals in Human Care. Animals, 14(6), 949. https://doi.org/10.3390/ani14060949
L 382-383 states: “In addition, the freezing and thawing of fish results in significant nutrient loss; for this reason supplements are often supplied (Brando et al., 2018).”
• This statement would benefit from clarification. Is the argument here that the animals are in fact getting their needs met, just in a different way than in the wild? Or are there data suggesting that even with supplementation, it is not possible to meet their nutritional needs in a facility?
L 390-396 states: “the routine consumption of readily available food sources, such as occurs in fish provisioning, ecotourism, or in the captive setting, does not satisfy the biological drive to engage complex cognitive and physical faculties inherent in foraging, which involves travelling to locate food along with capturing and consuming the prey. These activities present opportunities and challenges that are collectively enriching and consume a large percentage of cetaceans’ time budget in the wild (Neumann, 2001; Stockin et al., 2009; Noren & Hauser, 2016).”
• While the cited references report time spent traveling and foraging in wild cetaceans, they do not provide evidence or even suggest that these activities are inherently enriching or fulfill any needs beyond food acquisition. Inferring that behaviors are enriching solely based on the proportion of time animals spend engaged in them is unwarranted. Please either provide empirical evidence supporting the claim that these activities are enriching or revise the language to avoid attributing enrichment value based solely on activity budgets.
• Also, as before, the authors are overlooking or ignoring the animals’ cognitive and physical engagement in the positive reinforcement training sessions through which food is typically delivered in marine mammal facilities.
Lines 399–400 state: “Captive cetaceans are often required to interact with humans in different ways, for husbandry, training, and entertainment of the public – all of which have an effect on welfare.”
• In context, as currently written, the statement appears to suggest that these human-animal interactions are all or predominantly negative. In contrast, the Human–Animal Relationship (HAR) is recognized within the Five Domains model of animal welfare as a factor that can influence welfare both positively and negatively, depending on the nature of the interaction. For a more current perspective, please see Mellor et al. (2020).
o Mellor, D. J., Beausoleil, N. J., Littlewood, K. E., McLean, A. N., McGreevy, P. D., Jones, B., & Wilkins, C. (2020). The 2020 Five Domains Model: Including Human–Animal Interactions in Assessments of Animal Welfare. Animals, 10(10), 1870. https://doi.org/10.3390/ani10101870
L 421-424 states: “positive reinforcement methods in which the animals are rewarded with something they like, typically food, for performing a requested behavior. Trainers may also use a secondary reinforcer known as a “bridge”, usually a whistle, that indicates correct responses to a trainer’s commands (Feng et al., 2016).”
• The citation here is for clicker training with dogs. While related, there are some notable differences for training marine mammals, specifically with respect to the types of reinforcers that are typically used. A discussion of the basics of training as it is actually applied to marine mammals in facilities would be more appropriate here. For that, please see:
o Kuczaj, S. A., & Xitco Jr., M. J. (2002). It Takes More Than Fish: The Psychology of Marine Mammal Training. International Journal of Comparative Psychology, 15(2), 186–200. https://doi.org/10.46867/C4FK59
L 480–488 discusses the presence of illness, injury, and mortality in both captive and wild cetacean populations, and suggests that their presence in captivity may result from factors unique to that setting, such as stress, novel pathogens, and/or neurobiological harm. This argument is puzzling at best. Illness, injury, and mortality occur in all animal populations, including healthy and well-adapted ones. The relevant question, therefore, is the relative prevalence of these negative welfare states in facilities versus the wild.
L 532-535 states: “Miller et al. (2021) did not find a high rate of route tracing behavior (a form of stereotypical swimming) in the captive bottlenose dolphins they studied but rather a high rate of behavioral diversity, suggesting an inverse relationship between behavioral diversity and stereotypies.”
• In the context of the current discussion, the key takeaway from Miller et al. (2021) is less about this observed correlation and more about the extremely low occurrence of stereotypic behavior itself—particularly given that this study represents the largest multi-facility, international investigation of cetacean welfare to date. For a more accurate representation of stereotypic behavior prevalence in marine mammal facilities, I recommend emphasizing this point more directly and incorporating findings from Clegg et al. (2023b), already cited elsewhere in the manuscript, which reported that stereotypic behavior accounted for only 0.01% of the activity budget.
L 729-732 states: “However, the fact that these infant mortality statistics are the same in the wild and in captivity – where none of the dangers or risks inherent in the wild are present – leaves open the critical question of why neonatal deaths in captivity are not lower than in the wild”
• Please provide a reference for the data supporting this claim that infant mortality statistics are the same in the wild and in captivity (i.e., that neonatal deaths in captivity are in fact not lower than in the wild.)
L 766-770 states: “Estimates for free-living bottlenose dolphins suggest a maximum lifespan of ~25 years (Sergeant et al., 1973) whereas Wells et al. (2013) suggest an average age at death of 19.9 years. Wells & Scott (2009) suggest that female free-living bottlenose dolphins can live to more than 56 years and males to 48 years. Therefore, there is variation in estimates of maximum lifespan for free-living bottlenose dolphins.
• This section appears to conflate two distinct demographic metrics: “maximum lifespan” and “average age at death”. These are not interchangeable and should be clearly distinguished.
L 888–889 states: “more research is needed to determine if and how specific enrichment efforts can improve welfare.”
• This statement is inconsistent with the manuscript’s own earlier acknowledgment—just two paragraphs prior—that certain enrichment practices have already been shown to improve welfare. I recommend removing “if” and instead rephrasing to focus on clarifying how specific enrichment strategies contribute to welfare outcomes.
L 902-903 states: “These outcomes are in keeping with Mason’s (2010) study of how different species respond to captivity.”
• In that respect, it would seem worth noting here that Mason (2010) classified bottlenose dolphins as a “species with relatively good captive welfare”.
Lines 964–968 state: “although marine parks and aquariums can upgrade enclosures to offer some physical and behavioral benefit, they remain limited by available space and the artificial conditions required to keep cetaceans in captivity. Certainly, they cannot replicate the conditions of a free-living life necessary for cetaceans to truly thrive.”
In earlier comments, I noted that the manuscript asserts that cetaceans cannot thrive in captivity without ever defining what indicators or benchmarks would constitute “thriving.” Without articulating such criteria, it is not possible to evaluate whether this conclusion is supported by the available data.
Based on the current phrasing, it now appears that the authors may be taking the position that no welfare indicators—however positive—could ever demonstrate that cetaceans in captivity are thriving. If this interpretation is correct, I would respectfully point out that this moves the argument beyond the realm of scientific inquiry. Scientific conclusions must be grounded in hypotheses that are, at least in principle, falsifiable. If no set of empirical welfare data could challenge or revise the conclusion, then the argument is—by definition—a philosophical stance rather than an evidence-based scientific assessment.
To remedy this, I would again ask the authors to articulate what benchmarks one would need to see in order to show that cetaceans are thriving in captive situations (i.e., Even theoretically, even if contrary to expectations -- What is the actual bar?). From there, it would then become possible to assess the data regarding welfare indicators of the cetaceans in zoos and aquariums to see whether or not they meet those criteria.
Thank you for submitting this interesting review to PeerJ. I regret that I am unable to accept the manuscript for publication, at least in its present form. However, I am prepared to consider a new version that very carefully considers the many concerns highlighted by the reviewers. These need to be addressed comprehensively in a new version. Such a revised manuscript is likely to be reviewed again and there is no guarantee of acceptance. When you revise the manuscript, please prepare a detailed explanation about how you have dealt with all the reviewer comments.
**PeerJ Staff Note:** Please ensure that all review, editorial, and staff comments are addressed in a response letter and that any edits or clarifications mentioned in the letter are also inserted into the revised manuscript where appropriate.
[# PeerJ Staff Note: Reviewers 2 & 4 declared a potential Conflict of Interest, and the Editor was aware of this when making their decision #]
Thank you for the opportunity to review this manuscript. This paper is a scoping review that explores current knowledge on captive cetacean welfare, primarily focusing on literature published from 2000 to the present. The review can be of broad and cross-disciplinary interest and falls well within the journal's scope. However, as a minor comment that I would like to leave at the discretion of the editor and the authors, if it is absolutely needed or not, it may be useful to start the introduction with a more general context about animal captivity and animal welfare before "diving" into the specific case of cetaceans. Also, consider comparing their situation with that of non-cetacean species held in captivity, both in the discussion and the introduction.
As an exploration of current knowledge on captive cetacean welfare, particularly emphasizing the challenges and problems faced by the animals, I believe this work stands apart from previous reviews that have primarily focused on welfare assessment tools or ongoing efforts to enhance welfare.
The authors' motivation is well articulated.
The author performed a scoping review, which is appropriate given the complexity of the topic and the diverse approach, reporting, and methodologies available in the literature. For this reason, it is not necessarily a comprehensive review but can be informative for future, more systematic reviews, studies, or debates about cetacean welfare. I believe it is a timely review that can raise awareness of the inherent problem of holding cetaceans captive and invite further research and further consideration of the need for better regulation and policy.
Generally, the way the author structured the review is good. However, considering how important it is to them, I am surprised by the very little room given to talk about the acoustic aspect of cetacean life. By acoustic aspect, I am not only talking about the problem regarding their captive environment (e.g., noises) that the authors already pointed out, or their perception (echolocation), which is addressed briefly as well, but also whether their need to communicate acoustically and experience diverse sound is taken into consideration, and whether there has been any attempt to use their acoustic behavior to assess their well-being. Is it because the authors failed to include literature addressing these topics, or does it reflect one overlooked aspect of cetacean captive conditions? Either way, I believe the author can elaborate more on this aspect as it cannot be dissociated from anything cetacean.
The discussion and conclusion are appropriate. However, this is quite a dense manuscript, and by the time we arrive at the discussion section, the reader may have forgotten the main content of the previous sections. For this reason, adding more summaries of the key concepts and gaps from these sections in the discussion may help the readers. Please see some example suggestions on this in my line-by-line additional comments.
Additionally, I would like to point out that I personally appreciate that the authors end the paper with statements that highlight the direction for improving cetacean welfare, which questions the need for continuing to hold captive cetaceans, the consideration of moving towards the development of sanctuaries, and the need for building a list of species that are for sure should not be held captive anymore.
Line-by-line comments
Lines 51-52: The statement "has long been considered challenging" is true, and adding some references older than 2017 may be more supportive of this. Also, please remove the comma after "McGillian, 2023" in the following line.
Line 54: It is undoubtedly a popular film, but including more details that help locate and identify the source would be helpful (e.g., director, producer/distributor).
Line 71: Is it possible to indicate directly the reference/# of the decree issued by the authorities here instead of referencing a text from a news outlet (or include both)?
Lines 77-83: It would be helpful for readers to be introduced to the fact that there are two main groups of cetaceans (toothed vs. baleen whales) and that most captive animals are toothed whales, and the reason for that.
Line 131: How do you judge whether a paper is foundational?
Line 137: Maybe remove/change the "with" before "131 published …"
Lines 143-145: I am not sure to follow this sentence.
Lines 173-174: By reading this, it comes to my mind that it might be worth mentioning also in the intro that there were attempts to hold captive larger species (baleen whale calves, for instance). Moreover, here, clarify that you are talking about the largest among the species mentioned in the literature you included for the review.
Line 176: What does horizontal distance correspond to here? Diameter? Can you add more detail? Moreover, I believe you mean minimum horizontal dimension. Additionally, it would be helpful to include the section reference of the regulation/directive text to help readers locate this information.
Line 196: But activity level is not necessarily a sign of wellness, isn't it?
Line 212: Should you clearly mention echolocation when talking about perception and navigation? Given that you are, in the end, focusing on toothed whales.
Line 215: Also, the distance to the water surface and the bottom of the tank can be problematic, acoustically speaking, no?
Line 219: What do you mean by type of sociality?
Line 227: Can you include a reference here?
Line 244: Can we also say psychosocial?
Lines 248-249: Are there any sources for this?
Line 256: Can you provide examples of positive and negative welfare behaviors?
Line 262: What does "intricate" concretely mean in this sentence?
Line 267: How do you define high-quality food?
Line 275: I suggest adding a reference for this statement.
Lines 278-279: Can you also include references for this statement (about time budget)?
Lines 358-360: Can you include a date for this?
Line 472: Some number/percentage (quantitative data) like this would also be useful when you discuss the prevalence of the problems you report in some of your paragraphs. For example, when you say in line 466, "a common cause of mortality," to what extent is that? Likewise, in line 422.
Line 506: Did you specifically choose the term "lactation" because you want to say that the mother continues to produce milk for more than two years? I am asking because it does not necessarily imply that the young continue to feed on the milk during that time/not weaned. Otherwise, maybe formulate the sentence from the young's perspective by saying getting milk or something similar instead of the physiological state of the mother.
Line 525-526: Can you add some reference to this, even if you will develop it later in the following paragraph(s)?
Line 538: "parameters," such as?
Line 611: Can you briefly summarize these identified mismatches? By the time the readers arrive here, most have lost track of what was presented before, as it is a pretty dense manuscript.
Line 617: "further study is needed", like what?
Line 632: Can you talk a bit about these exceptions? Mainly, why did they work? I think it is an essential point to keep in mind, as sometimes we assume by default that there is no way/no case where releasing captive animals can work.
Wishing you the best.
BASIC REPORTING:
Note: Given the volume of necessary edits, I have made an editable version of this manuscript and placed comments within. Comments for how to improve a potential revision are included in that attachment.
Is the review of broad and cross-disciplinary interest and within the scope of the journal?
It seems the topic of cetacean captivity is within the scope of the journal.
I do not know exactly how broad the cross-disciplinary interest will be given cetacean captivity issues are fairly niche in scientific community. Online and in social media articles like this are used frequently to advocate for anti-captivity positions so it may have legs there.
Has the field been reviewed recently? If so, is there a good reason for this review (different point of view, accessible to a different audience, etc.)?
I think the best review of cetacean captivity (with data) is The Cetacean Welfare Study led by Lance Miller. This is a nine-paper series using the latest technology and tools to assess captive cetacean welfare across almost every accredited facility in the US and Europe. https://collections.plos.org/collection/cetacean-welfare/ This review barely mentions this comprehensive series of studies and seems more focused on presenting a narrative favorable to cetacean sanctuary projects. That would be fine if this took an even and comprehensive position relative to the literature. Unfortunately, this manuscript fails to do that in a meaningful way (see Attachments for line-by-line examples of these shortcomings). As such this reads very much like previous articles from these authors (Marino et al 2020 and Jacobs et al 2021) that each have comprehensive rebuttals from many groups of authors. I don't honestly know what the purpose of this paper is in terms of the scientific literature.
Does the Introduction adequately introduce the subject and make it clear who the audience is/what the motivation is?
The Introduction does not adequately introduce the subject as the authors present a fairly biased interpretation of current captive situations (see Additional Documents for specific examples). Frankly, given the seminal nature of The Cetacean Welfare Study on this topic if the authors aren't going to frame this paper as either a rebuttal or comprehensive assessment of those conclusions then I don't know how this can either provide a reasoned different view of the state of information for captive cetaceans or even inform a different audience about the current state of information in captive cetaceans. I don't know what the motivation for this paper is considering the author's stated goals relative to their execution of said goals though their limited evaluation of the scientific data on cetacean welfare (specifically studies that show positive welfare gains- see attachments).
Is the Survey Methodology consistent with a comprehensive, unbiased coverage of the subject? If not, what is missing?
No. For example. The Survey Methodology describes an arbitrary process where the authors state that papers published before 2000 would not be considered unless they were foundational papers. However, I would argue that not only are many of the pre-2000 papers not foundational, but they all seem to lean toward an anticaptivity bent. I can see Mason, 1991 but most of the others seem not to be foundational papers. The reliance on biased non-peer reviewed sources like Vail (which is not accessible https://us.whales.org/2012/12/03/the-mixed-messages-of-captivity/) or Long 2018 https://us.whales.org/2018/08/23/how-long-do-bottlenose-dolphins-survive-in-captivity/) is problematic because while these poorer blog sources support anti-zoo narratives they are used in place of quality peer reviewed work that shows zoos more positively. sources. Like this for lifespan data https://royalsocietypublishing.org/doi/10.1098/rspb.2023.1895.
Are sources adequately cited? Quoted or paraphrased as appropriate?
No. Please see the attachments. Many examples of misrepresented research. This work is not in keeping with the standards of PeerJ.
Is the review organized logically into coherent paragraphs/subsections?
There is a great deal of repetition where concepts like stereotypical behaviors are brought up throughout with little organization.
Is there a well developed and supported argument that meets the goals set out in the Introduction?
Not with this level of bias, no. This is not an assessment of the current state of cetacean captivity (that would be The Cetacean Welfare Study). This is a remix of Marino et al, 2020 and Jacobs, et al,. 2021 and it lacks a fulsome review of the literature, both in terms of challenges for zoos as well as the challenges zoos have overcome.
Does the Conclusion identify unresolved questions / gaps / future directions?
The conclusions and ideas for moving forward are also not well organized and seem muddled in focus. There should be specifically a section that considers paths moving forward, especially in the assessment of if sanctuaries would be effective for improving welfare. instead of discussing the challenges associated with a sanctuary, something the lead author should be familiar with, sanctuaries are offered as a panacea, unchallenged. It gives the appearance of self-interested bias, and is a missed opportunity to highlight the sober knowledge the WSP has gained since it began its efforts in 2016.
See Attachment
This review is incredibly well written and conceived. It provides a comprehensive overview of the welfare issues surrounding the keeping of cetaceans in captivity and is a timely update to this situation. I believe this will be of interest to all animal welfare scientists and to the genera public.
As this is a review the authors outline their approach to including published material for inclusion. Their method is clearly laid out.
L130 What does readable in full mean? Open access? Or the paper was not in English?
L139 websites - are these all referenced or should they be listed in Supplementary Information?
The authors review the main aspects that affect welfare of captive cetaceans providing insights into those contexts which influence the welfare and health of these animals.
L160 Can you provide % of animals in land-based concrete tanks?
L64 can you define logging?
L381 There have been quite a few attacks on boats by orcas in the Mediterranean recently - are you defining these as boats and not direct human attacks? Perhaps comment on this - it has received much media attention.
L609 I wonder if the authors could discuss rehoming in greater detail. Currently there is a problem with two orcas in Antibes where it is becoming impossible to find them a suitable home/sanctuary - see https://www.france24.com/en/europe/20250411-rights-group-urges-france-to-move-orcas-to-sanctuary-after-spain-refused-transfer. So the problem of dealing with these animals is rather political as well as welfare relevant. Transferring them to a sanctuary as outlined in your discussion would seem the most appropriate course of action but their fate remains in the balance. I think this would make a useful addition to your discussion.
Minor comments:
L511 delete "as well" please
L572 Please replace "Copious" with "Many"
This review is similar in substance to two other reviews by some of the same authors in recent years, with largely the same arguments and conclusions.
• Jacobs, B., Rally, H., Doyle, C., O’Brien, L., Tennison, M., & Marino, L. (2022). Putative neural consequences of captivity for elephants and cetaceans. Reviews in the Neurosciences, 33(4), 439–465. https://doi.org/10.1515/revneuro-2021-0100
• Marino, L., Rose, N. A., Visser, I. N., Rally, H., Ferdowsian, H., & Slootsky, V. (2020). The harmful effects of captivity and chronic stress on the well-being of orcas (Orcinus orca). Journal of Veterinary Behavior, 35, 69–82. https://doi.org/10.1016/j.jveb.2019.05.005
To avoid the possibility or impression of duplication, I would suggest that the authors explain how the data and/or their conclusions have evolved since these earlier reviews, creating a need for this additional review of the topic.
In either case, I applaud the authors’ stated intention to provide “an accurate, comprehensive and current picture of the status of captive cetaceans” [L. 143]. This is a laudable goal that certainly falls within the scope of this journal. That said, however, the current manuscript unfortunately falls short of this goal in a number of ways. (See below)
The current manuscript does not give an accurate review of the scientific literature on this topic. There are numerous instances where: (a) the references cited do not support the data or claims attributed to them; (b) directly relevant references that should be cited are omitted from the discussion; and/or (c) supporting evidence is presented from a cited reference, while potentially opposing evidence from that same reference is omitted. For example:
L 172-3 states: “There is considerable variation in tank size across facilities. Many tanks are too small or shallow to allow natural swimming behaviors (McPhee & Carlstead, 2010).”
• McPhee & Carlstead (2010) does not say this (or even mention cetaceans).
• For data on size of enclosures that would be relevant here, please see: Lauderdale, L. K., Walsh, M. T., Mellen, J. D., Granger, D. A., & Miller, L. J. (2021). Environmental enrichment, training, and habitat characteristics of common bottlenose dolphins (Tursiops truncatus) and Indo-Pacific bottlenose dolphins (Tursiops aduncus). PLoS ONE, 16(8), e0253688.
L 299-311. In the discussion of whether swim-with-dolphins (SWD) programs are stressful or otherwise negative for the animals:
• The authors state that “several factors may play an important role in cortisol (stress hormone) levels during these interactive programs (Matsushiro et al., 2021)”, while omitting the result from this paper that dolphins had lower cortisol levels after participating in swim programs. Given that they interpret higher cortisol levels as indicators of increased stress elsewhere in this manuscript, presumably these lower levels should correspondingly be interpreted as an indicator of decreased stress.
• A well-known and relevant paper with contradictory data is omitted (Miller, L., Mellen, J., Greer, T., & Kuczaj, S. A. I. (2011). The effects of education programmes on Atlantic bottlenose dolphin (Tursiops truncatus) behaviour. Animal Welfare, 20, 159–172). This paper found higher rates of behavioral diversity following swim programs, a measure which is typically interpreted as a positive indicator of animal welfare.
L 377-378. The suggestion that serious aggression is unusual in wild cetaceans is not correct. The authors cite two papers about killer whale behavior (one of which details a case of infanticide), and omit any references about dolphin aggression (which is a well-known and natural part of their social interactions). See, e.g.,
• Dunn, D.G.; Barco, S.G.; Pabst, D.A.; McLellan, W.A. Evidence for Infanticide in Bottlenose Dolphins of the Western North Atlantic. J. Wildl. Dis. 2002, 38, 505–510.
• Marley, S.A.; Cheney, B.; Thompson, P.M. Using Tooth Rakes to Monitor Population and Sex Differences in Aggressive Behaviour in Bottlenose Dolphins (Tursiops truncatus). Aquat. Mamm. 2013, 39, 107–115.
• Parsons, K.M.; Durban, J.W.; Claridge, D.E. Male-Male Aggression Renders Bottlenose Dolphin (Tursiops truncatus) Unconscious. Aquat. Mamm. 2003, 29, 360–362.
• Robinson, K.P. Agonistic Intraspecific Behavior in Free-Ranging Bottlenose Dolphins: Calf-Directed Aggression and Infanticidal Tendencies by Adult Males. Mar. Mammal Sci. 2014, 30, 381–388.
• Scott, E.M.; Mann, J.; Watson-Capps, J.J.; Sargeant, B.L.; Connor, R.C. Aggression in Bottlenose Dolphins: Evidence for Sexual Coercion, Male-Male Competition, and Female Tolerance through Analysis of Tooth-Rake Marks and Behaviour. Behaviour 2005, 142, 21–44.
L 385-8 states: “captive bottlenose dolphins and other cetaceans, especially those in petting and feeding sessions with the public and SWD programs, also have a long record of aggression towards humans, often resulting in severe human injuries (Shane et al., 1993; Spradlin et al., 1999; Vail, 2012; Anderson et al., 2016;)”
• The Shane et al. (1993) and Spradlin et al. (1999) articles are about interactions with wild cetaceans; not captive ones.
• Vail (2012) is apparently a blog post that is no longer available.
L 531-2 states: “Estimates for free-living bottlenose dolphins suggest a mean life expectancy of ~25 years (Sergeant et al., 1973; Wells et al., 2013) and a maximum of ~50-70 years (Wells & Scott, 2009).”
• The “25 years” figure in Sergeant et al. (1973) refers to the maximum lifespan they found; not the mean life expectancy.
• The average age at death figure in Wells et al. (2013) is 19.9 years. (They didn’t calculate a mean life expectancy.)
• Wells & Scott (2009) says that “female common bottlenose dolphins can live to more than 57 years, and males up to 48 years”
L 533-534 states: “One recent study suggested that mean life expectancy for captive bottlenose dolphins is not significantly different from that in some free-living populations (Jaakkola & Willis; 2019).”
• This is misleading. Jaakkola & Willis (2019) found that recent survival rates (and therefore life expectancies) were numerically higher in captivity than in all three wild populations for which comparable data are available, with two out of the three significantly higher.
• The authors also omitted the most recent scientific paper on this topic – Tidière et al. (2023). Survival improvements of marine mammals in zoological institutions mirror historical advances in human longevity. Proceedings of the Royal Society B: Biological Sciences, 290(2009), 20231895. https://doi.org/10.1098/rspb.2023.1895 -- which found that for the past several decades, life expectancy for captive bottlenose dolphins has been significantly higher than for wild dolphins.
• Instead of these peer-reviewed references, the authors base their conclusions on a blog post from an undergraduate two-week project, in which the analyses are not appropriate for the argument being made (See General comments below).
L 544-548. In their discussion about life expectancy of captive orcas, the authors omit any discussion of the scientific papers that have been published on this topic (which they have cited in previous reviews).
• Robeck, T. R., Willis, K., Scarpuzzi, M. R., & O’Brien, J. K. (2015). Comparisons of life-history parameters between free-ranging and captive killer whale (Orcinus orca) populations for application toward species management. Journal of Mammalogy, 96(5), 1055–1070. https://doi.org/10.1093/jmammal/gyv113
• Jett, J., & Ventre, J. (2015). Captive killer whale (Orcinus orca) survival. Marine Mammal Science, 31(4), 1362–1377. https://doi.org/10.1111/mms.12225
There are a number of misleading arguments throughout the manuscript, including:
A) L 87-93. The authors first mention one out of several accrediting organizations, saying: “Accrediting organizations (e.g., Association of Zoos and Aquariums, AZA) set welfare standards for the zoological industry”. They then argue that because “only a relatively small number of existing zoos and aquatic parks around the world are accredited by” that one accrediting organization, this “ point(s) to widespread problems in welfare standards for the majority of captive entertainment facilities”. In point of fact, there are multiple accrediting organizations that set welfare standards across the world. To argue that most facilities aren’t accredited (and therefore have problems in welfare standards), one would need to include more than a single accrediting organization.
B) L 175-7 states: “the United States Department of Agriculture.s (USDA) minimum size standard for orca enclosures is 15 m for horizontal distance and 4 m for depth, severely limiting natural movements, postures, and behaviors.”
• Measurements of minimum legal space are not the same as measurements of the space in which the animals are actually housed. The relevant data for assessing welfare must be how the animals are actually housed, as this is the factor that could impact the animals.
C) Similarly, the authors occasionally listed potential welfare considerations as if they were actual systematic welfare problems, without presenting or referencing data regarding the prevalence of the issue in the lives of the cetaceans under consideration. E.g.,
• “Excessive chlorination can cause skin and eye problems in marine mammals (Gage & Francis-Floyd, 2018).” (L 208-9)
• “Persistent, anthropogenic noise from nearby construction, traffic or amusement park rides, if not dampened sufficiently, can increase stress and negatively impact welfare, i.e., increase levels of cortisol (Yang et al., 2021).” (L 212-14)
As written, these statements are certainly true, but the relevant question for assessing welfare would be the extent to which the animals are exposed to these conditions, which they authors never discuss. (In the same way that one might note that a lack of food will cause animals to starve, without engaging in the question of how much the animals are actually being fed).
D) L 493-5 states: “Most cases of neonatal death in captive facilities occur in young females giving birth for the first time (Owen, 1990; Sweeney et al., 2010), which may be due to immaturity and lack of exposure to natural mother-calf relationships (i.e., factors particularly relevant to the captive situation).” – The authors fail to note, however, that this difference in death rates for first-born versus later-born calves is also true in the wild. See, e.g.,
• Henderson, S. D., Dawson, S. M., Currey, R. J. C., Lusseau, D., & Schneider, K. (2014). Reproduction, birth seasonality, and calf survival of bottlenose dolphins in Doubtful Sound, New Zealand. Marine Mammal Science, 30(3), 1067–1080. https://doi.org/10.1111/mms.12109
• Robinson KP et al. 2017 Female reproductive success and calf survival in a North Sea coastal bottlenose dolphin (Tursiops truncatus) population. PLoS ONE 12, e0185000. (doi:10.1371/journal.pone.0185000)
• Wells, R. S., Hohn, A. A., Scott, M. D., Sweeney, J. C., Townsend Jr, F. I., Allen, J. B., ... & Irvine, A. B. (2025). Life history, reproductive, and demographic parameters for bottlenose dolphins (Tursiops truncatus) in Sarasota Bay, Florida. Frontiers in Marine Science, 12, 1531528.
Thus, a situation is being attributed to “captivity” that is simply true of cetaceans in general.
L 625-632. The authors’ contention that it is not possible to meet the conditions for cetaceans to thrive in marine parks and aquariums is undermined by the fact that they never articulate what welfare measures one would theoretically need to meet in order to show whether the animals are in fact thriving. Without that, it is impossible to reach a scientific conclusion based on an objective review of the data. To remedy this, I would ask the authors to articulate what benchmarks one would need to see in order to show that cetaceans are thriving in captive situations (i.e., Even theoretically, even if contrary to expectations -- What is the actual bar?). From there, it would then become possible to assess the data regarding welfare indicators of the cetaceans in zoos and aquariums to see whether or not they meet those criteria.
L 295 states: “There are no specific regulations that safeguard animal well-being in interactions with visitors”, while L 297-8 states that “limited regulations governing swim-with-dolphins (SWD) programs exist under the U.S. Animal Welfare Act. These statements seem contradictory. Can you clarify?
L 349-353 states: “Also found in captive cetaceans are circling and repetitive swimming patterns (Jett & Ventre, 2011; Ugaz et al., 2013). However, Miller et al. (2021) did not find a high rate of route tracing behavior (a form of stereotypical swimming) in the captive bottlenose dolphins they studied but rather a high rate of behavioral diversity, suggesting an inverse relationship between behavioral diversity and stereotypies.”
• A number of welfare scientists have questioned whether this behavior is actually a stereotypy (e.g., Brando et al., 2018; Clark, 2013; Clegg & Delfour, 2018). Please include this in your discussion.
o Brando, S.; Broom, D.M.; Acasuso-Rivero, C.; Clark, F. Optimal Marine Mammal Welfare under Human Care: Current Efforts and Future Directions. Behav. Process. 2018, 156, 16–36.
o Clark, F.E. Marine Mammal Cognition and Captive Care: A Proposal for Cognitive Enrichment in Zoos and Aquariums. J. Zoo Aquar. Res. 2013, 1, 1–6.
o Clegg, I.L.K.; Delfour, F. Can We Assess Marine Mammal Welfare in Captivity and in the Wild? Considering the Example of Bottlenose Dolphins. Aquat. Mamm. 2018, 44, 181–200.
• As you are prioritizing to the most recently dated findings (L 136), presumably the multi-facility welfare study reported in Miller et al. (2021) should be particularly meaningful. A more accurate description of their findings would note not just that they “did not find a high rate” of this behavior, but that in fact this behavior was extremely rare (i.e., an average of 0.0 times per minute).
• When you mention behavioral diversity, it would be helpful to contextualize this by noting that this is considered an indicator of positive welfare. e.g.,
o Brereton, J. E., & Fernandez, E. J. (2022). Investigating Unused Tools for the Animal Behavioral Diversity Toolkit. Animals, 12(21), 2984. https://doi.org/10.3390/ani12212984
o Miller, L. J., Vicino, G. A., Sheftel, J., & Lauderdale, L. K. (2020). Behavioral Diversity as a Potential Indicator of Positive Animal Welfare. Animals, 10(7), 1211. https://doi.org/10.3390/ani10071211
L 496–522. It is not clear what argument is being made with respect to artificial insemination. AI is generally considered a standard husbandry practice, used safely and effectively with many species around the world. Is the argument here that AI is typically done poorly with cetaceans, and is therefore a welfare risk? Or that AI itself is inherently associated with poor welfare? Or something else? Please clarify and provide references for whatever welfare argument is meant here.
L 533-534 states: “Moreover, when other parameters are examined, captive dolphins fare more poorly. For instance, mean survival time in captivity (for dolphins who live more than one year) across 67 facilities in the U.S. and Europe has been estimated to be only 12.75 years, with mortality rate twice as high in captive bottlenose dolphins compared to free-
living dolphins (Long, 2018).”
• The reference here is for a blog post describing a two-week project from an undergraduate student. This is not a legitimate scientific study to cite.
• In addition, for what it is worth, the data analyzed are from 1939 – 2018. Given that life expectancy for dolphins in captivity has approximately tripled in the last 40 years (Jaakkola & Willis, 2019; Tidière et al., 2023), the early data are very much out of date and not representative of the current status. If your goal is to provide “an accurate, comprehensive and current picture of the status of captive cetaceans” (L 143), it is the current status that is relevant, as presented in both peer-reviewed studies on this topic (Jaakkola & Willis, 2019; Tidière et al., 2023).
• Also, for what it is worth, the student did not in fact calculate mortality rate for this captive population, nor statistically compare it to a wild population.
L 598-9 states: “with the caveat that certain aspects of enrichment (e.g., space) cannot reasonably be addressed in traditional captive facilities”
• Please include an explanation of what data led you to this conclusion. If true, this is certainly worth noting. However, it doesn’t seem to follow from any data you have presented in this review. This is generally considered a complex issue, given that multiple welfare papers (including some in your reference list, e.g., Lauderdale et al., 2021c; McPhee & Carlstead, 2010; Morgan & Tromborg, 2007) have noted that the quality and management of an animal’s enclosure is often more important for animal well-being than the physical measurements of the space. Please include this in your discussion to clarify your reasoning.
L 604-7 states: “However, whereas some enrichment methods may appear to contribute to improved welfare, there is no evidence to suggest that currently employed methods allow captive cetaceans to actually thrive or that positive effects are maintained over the long term (Delfour et al., 2017).
• What criteria are you using to distinguish between something that “appears to” contribute to improved welfare versus actually contributes to improved welfare?
• Similarly, how are you defining “actually thrive”? That is, what sort of evidence would you need to see in order to conclude that captive cetaceans are “actually thriving”?
• The Delfour et al. (2017) article was an observational study that examined dolphins’ reactions to provided objects. Their main result was “In general, subjects preferred the objects classified as simple and floating, they displayed a larger variety of behaviours, they spent more time and were more creative with them than with other types of objects.” On my reading, this article does not seem to say what is being attributed to it here. Please clarify what part of this article led you to this conclusion.
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