Physiological, Behavioral, and Scientific Impact of Different Fluid Control Protocols in the Rhesus Macaque (Macaca mulatta)
Abstract
Rhesus macaques are an important model in behavioral neuroscience due to their advanced cognitive abilities. To motivate animals to engage in complex tasks, fluid rewards, in conjunction with fluid control protocols, are often used. The impact of these protocols on animal welfare is controversial. We compared two fluid control protocols against a protocol providing free access to water and evaluated the impacts on physiological states of hydration, behavioral measures of welfare, and scientific output. Blood physiology did not significantly differ between any of the protocols, and urine measures were indicative of well functioning, healthy kidneys. Changes in behaviors were limited, the main one being an increase in motivation to drink on the stricter fluid control protocol, and improved task performance early in the week. Overall, fluid control protocols had little measurable impact on the welfare of rhesus macaques while ensuring that scientific data of high quality could be obtained.
Footnotes
The authors declare no competing financial interests.
The work was supported by the NC3Rs (Grant NC/K500410/1) and the Wellcome Trust. The internet Primate Aging Database (iPAD) is supported by contract HHSN271201300026C from the National Institute on Aging/National Institutes of Health to Dr. Joseph W. Kemnitz at the Wisconsin National Primate Research Center, University of Wisconsin-Madison.
This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International, which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.
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- Author ResponseHelen Gray, Henri Bertrand, Paul Flecknell, Candy L Rowe and Alexander ThielePublished on: 25 April 2017
- RE: Physiological, behavioral, and scientific impact of different fluid control protocols in the rhesus macaque (Macaca mulatta) – Gray et al. 2016 eNeuro 0195-16.2016Penny Hawkins, Ros Clubb, Sarah Wolfensohn and Michelle Hudson-SHorePublished on: 16 January 2017
- Published on: (25 April 2017)Page navigation anchor for Author ResponseAuthor Response
- Helen Gray, PhD, University of Leeds
- Other Contributors:
- Henri Bertrand
- Paul Flecknell
- Candy L Rowe
- Alexander Thiele
The eLetter by Hawkins et al. makes a variety of sweeping, unsubstantiated comments. It has neither been peer reviewed nor has it undergone editorial scrutiny. It does not provide sufficiently specific scientific arguments, which makes it impossible to engage in an adequate scientific discussion. However, the little there is, can be addressed:
Our hypotheses and aims were clear, and in response to an NC3Rs Working Group that highlighted that: ‘Of particular value would be a comparison of protocols currently approved in the UK in which monkeys may perform the experimental task to obtain fluid 5 or 6 days a week…compared with protocols which involve working every day for longer periods…’ (Prescott et al. 2010). To address this, we provide the first scientific data comparing these protocols, measuring both performance in a cognitive task and welfare impacts using a battery of physiological and behavioural measures.
The choice of control period is criticized, as monkeys had free access to water over the Christmas break, while not performing experiments. It is argued that this change in routine could have affected their behavior, explaining why little difference in behaviour occurred between this period and when animals were under a fluid control regime. However, this interpretation would imply that the fluid control regime had the same welfare impact as a break from experimental protocols wi...
Show MoreThe eLetter by Hawkins et al. makes a variety of sweeping, unsubstantiated comments. It has neither been peer reviewed nor has it undergone editorial scrutiny. It does not provide sufficiently specific scientific arguments, which makes it impossible to engage in an adequate scientific discussion. However, the little there is, can be addressed:
Our hypotheses and aims were clear, and in response to an NC3Rs Working Group that highlighted that: ‘Of particular value would be a comparison of protocols currently approved in the UK in which monkeys may perform the experimental task to obtain fluid 5 or 6 days a week…compared with protocols which involve working every day for longer periods…’ (Prescott et al. 2010). To address this, we provide the first scientific data comparing these protocols, measuring both performance in a cognitive task and welfare impacts using a battery of physiological and behavioural measures.
The choice of control period is criticized, as monkeys had free access to water over the Christmas break, while not performing experiments. It is argued that this change in routine could have affected their behavior, explaining why little difference in behaviour occurred between this period and when animals were under a fluid control regime. However, this interpretation would imply that the fluid control regime had the same welfare impact as a break from experimental protocols with free access to water. As anyone working with primates knows, it is impossible to run a normal experimental routine with an animal on free access to water. We maintain that our control period allows for useful and valid comparisons to be made.
Hawkins et al also complain that insufficient methodological details are provided to enable the study to be repeated, i.e. non-compliance with the ARRIVE guidelines. We made considerable effort to follow the guidelines, and note that many of the details claimed to be missing are actually included in the manuscript (e.g. details of the housing facility).
We do not agree that ‘potential confounds’ require further discussion, and do not accept, for example, that the type of fluid reward received could be considered a confound in our experiments. We also disagree with the implicit argument that the behavioural measures were inadequate. We carried out extensive consultation with experts in macaque welfare and behaviour to select these indicators. These experts were proposed by the NC3Rs, and all of the welfare measures used were extensively discussed with them and the NC3Rs to ensure that they were appropriate.
We set out to give an objective evaluation of the impact of two fluid control protocols, and our conclusions are adequate given the evidence. Our results may be challenging, since they do not support current welfare concerns around the use of these fluid control protocols, but alternative viewpoints should be supported by sound scientific data. The eLetter by Hawkins et al. simply attempts to dismiss and discredit the evidence, for what appear to be ideologically and politically motivated reasons.
Show LessCompeting Interests: None declared. - Published on: (16 January 2017)Page navigation anchor for RE: Physiological, behavioral, and scientific impact of different fluid control protocols in the rhesus macaque (Macaca mulatta) – Gray et al. 2016 eNeuro 0195-16.2016RE: Physiological, behavioral, and scientific impact of different fluid control protocols in the rhesus macaque (Macaca mulatta) – Gray et al. 2016 eNeuro 0195-16.2016
- Penny Hawkins, Head, Research Animals Department, RSPCA
- Other Contributors:
- Ros Clubb
- Sarah Wolfensohn
- Michelle Hudson-SHore
Penny Hawkins, Ros Clubb, Sarah Wolfensohn, and Michelle Hudson-Shore
Behavioural neuroscience studies using non-human primates, particularly long-term protocols involving complex tasks, raise significant ethical and animal welfare concerns that are shared by the public and the scientific community. Fluid restriction, which is commonly used to motivate primates to perform behavioural tasks, presents an additional concern because it can increase the cumulative effects of procedures.
It is therefore essential to evaluate the physiological and psychological impacts of these studies, to improve the ability to recognise (and alleviate) suffering and better inform the harm-benefit analysis before, during and after these projects are conducted. However, we have concerns about the methodology and conclusions of this paper. For example, there does not appear to be a clear hypothesis, the ‘control’ group is not strictly a control, there is insufficient information in the methods section to replicate the study, and potential confounds could have been better acknowledged and discussed. Some groupings of behavioural indicators could lead to misinterpretation of the data, and there is no convincing assessment of the animals’ psychological wellbeing; a critically important factor.
We believe that the conclusions, drawn using data from just four animals, are not sustainable and should have been far more tentative; for example, by presenting this as a pilot study...
Show MorePenny Hawkins, Ros Clubb, Sarah Wolfensohn, and Michelle Hudson-Shore
Behavioural neuroscience studies using non-human primates, particularly long-term protocols involving complex tasks, raise significant ethical and animal welfare concerns that are shared by the public and the scientific community. Fluid restriction, which is commonly used to motivate primates to perform behavioural tasks, presents an additional concern because it can increase the cumulative effects of procedures.
It is therefore essential to evaluate the physiological and psychological impacts of these studies, to improve the ability to recognise (and alleviate) suffering and better inform the harm-benefit analysis before, during and after these projects are conducted. However, we have concerns about the methodology and conclusions of this paper. For example, there does not appear to be a clear hypothesis, the ‘control’ group is not strictly a control, there is insufficient information in the methods section to replicate the study, and potential confounds could have been better acknowledged and discussed. Some groupings of behavioural indicators could lead to misinterpretation of the data, and there is no convincing assessment of the animals’ psychological wellbeing; a critically important factor.
We believe that the conclusions, drawn using data from just four animals, are not sustainable and should have been far more tentative; for example, by presenting this as a pilot study to help develop the protocol for evaluating the impact of fluid restriction. We agree with the NC3Rs that further research is needed, e.g. as an international, multi-centre study.
For further explanation and discussion of the above, please see http://tinyurl.com/gv4gpxr
Show LessCompeting Interests: None declared.