ABSTRACT

Over several decades, animal welfare has grown into its own free-standing field of scientific study, from its early beginnings in laboratory animal research to eventually include exhibited animals and farm animals. While it has always been present to some degree, consideration of animal welfare for free-ranging animals has lagged behind, developing as a field of study in the last 20 yr or so. Part of that increase was that animal welfare legislation was finally applied to studies being done on free-ranging animals. But it is the appreciation by the biologists and veterinarians working on wild animals, in which the quality of their results is largely controlled by the quality of the animals they use in their studies, which has resulted in increased attention to the well-being or welfare of the animals that they use. Other important influences driving the recognition of wildlife welfare have been changes in the public's expectations of how wild animals are dealt with, a shift in focus of wildlife professionals from managing animals that can be hunted or angled to include nongame species, the decrease in participation in hunting and fishing by members of the public, and the entry of large numbers of women into fish and wildlife agencies and departments and into veterinary medicine. Technical improvements have allowed the safe capture and handling of large or dangerous animals as immobilization drugs and equipment have been developed. The increasing use of sedating drugs allows for handling of animals with reduced stress and other impacts. A number of topics, such as toe-clipping, branding, defining which taxa can or cannot feel pain, catch-and-release fishing, and more, remain controversial within wildlife science. How we treat the wild animals that we deal with defines who we are as wildlife professionals, and animal welfare concerns and techniques for free-ranging animals will continue to develop and evolve.

INTRODUCTION

Wild animals fascinate people. Witness the many television shows highlighting wild animals as evidence of the popularity of free-ranging animals with the general public. The public is generally supportive of research done on wild animals but has high expectations of how such research is conducted and how wild animals are treated by researchers and managers. The public views wild animals as individuals whereas wildlife professionals tend to view wildlife as populations, which can sometimes lead to controversy. Mentioning the phrase “animal welfare” in relation to wildlife does not represent an accusation or an indictment of the work being done any more than discussing the suitability of the techniques used to gather data or the statistical methods used to analyze them does so. Scientific peer reviews of proposals and publications act as a quality control review of scientific adequacy. Reviews by an Animal Ethics Committee or Institutional Animal Care and Use Committee act as quality control on the use and treatment of animals used in research. Researchers themselves have questioned some conservation projects as being poor science, with animal welfare concerns knowingly or unknowingly at issue (Frank 2013).

What is animal welfare?

Many definitions of animal welfare exist. Perhaps the simplest and most inclusive definition is that offered by the American College of Animal Welfare (ACAW): “Animal welfare refers to the state of the animal. Assessment of welfare includes consideration of the animal's health, behavior, and biological function.” (ACAW 2015). In essence, anything that might contribute to or detract from the normal state of the animal is an animal welfare issue. During research or management actions on wild animals, the main activities that potentially affect animal welfare are chase, capture, restraint, handling, holding, transportation, and procedures directly applied to the animals (e.g., sampling of blood, hair, saliva, or feather, attachment of transmitters or data loggers, tagging or banding, surgery, toe-clipping). There are very few research and management actions that do not have the potential, in some way, for affecting the animals being studied. Even projects that simply observe wild animals can sometimes have an adverse effect (e.g., Carey 2011; McMahon et al. 2012; Zommers et al. 2013).

Why wild animal welfare now?

As a well-established field of both concern and study in laboratory animal medicine, animal welfare has a literature base specific to it (Walker et al. 2014). Animal welfare has only been considered seriously in the fish and wildlife fields in recent years, as reflected by the rapid increase in publications reflecting that concern directly (Fig. 1). That is not to say that wildlife biologists and veterinarians were previously unaware of the effects of their activities on their study animals. The wildlife scientific literature is replete with reports of the presence or absence of adverse effects of field procedures on animals. These reports are evidence of the conscious recognition by wildlife researchers that the welfare of their animals has a direct effect on the quality of the resulting data they are gathering. It is the issue of data quality that links animal welfare as of direct importance to wildlife research and management and is the basis of developing animal welfare as a field of study for wild animals.

Figure 1. 

Bibliographic analysis of the appearance from 1985 to 2014 of publications on fish (black circles) and wildlife (white circles) specifying animal welfare as a topic. The data were gathered using the Scopus® search engine (http://www.scopus.com/), accessed May 2014, using “animal welfare” and “fish” or “wildlife” as keywords in separate searches of the years 1985–2014.

Figure 1. 

Bibliographic analysis of the appearance from 1985 to 2014 of publications on fish (black circles) and wildlife (white circles) specifying animal welfare as a topic. The data were gathered using the Scopus® search engine (http://www.scopus.com/), accessed May 2014, using “animal welfare” and “fish” or “wildlife” as keywords in separate searches of the years 1985–2014.

Animal welfare legislation now exists in most developed countries with varying coverage of fish and wildlife activities. In the United States, the Animal Welfare Act (7 U.S.C. 2131 et seq.) and its enabling regulations (CFR Title 9) have been in force for decades (see Cardon et al. 2012), although coverage of some taxa and some research organizations has been uneven in regulations (Mulcahy 2003). Perhaps more influential in increasing compliance with animal welfare regulations has been the requirement for animal ethics committee review of projects before collection permits are issued and before the resulting manuscripts are considered for publication by journals.

Entry of women into wildlife biology

One of the most-positive influences on the welfare of free-ranging animals has been the entry of women in large numbers into the fish and wildlife fields. Elizabeth Beard Losey was the first female wildlife biologist to become a member of The Wildlife Society and, in 1946, the first to be hired by the US Fish and Wildlife Service (Casselman 2006). In 1944, only 2% of the members of The Wildlife Society were women, a number that increased to 22% in 2006 (Nicholson et al. 2008). But women have always contributed to the growth of wildlife scientific knowledge in excess to their proportion: 8.3% of papers appearing in the Journal of Wildlife Management in 1937 had a female author; in 2006 the contribution had grown to 45% (Nicholson et al. 2008). Gender is one of the most important indicators of a person's attitudes and opinions about animals, including wild animals (Kellert and Berry 1987; Herzog et al. 1991). Generally, women's views on wildlife issues differ from men's, and women better maintain their views over time (Butler et al. 2003). Female veterinary students have higher “empathy scores” than do male students, and that difference is maintained throughout the veterinary educational process (Paul and Podberscek 2000; Pollard-Williams et al. 2014). A similar gender divergence is also seen in nonveterinary university students (Phillips et al. 2010). The entry of women into the fields of fish and wildlife research and management means that their more-empathetic views about animals, as well as a tendency towards greater emphasis on communication about wildlife and less-consumptive uses of wildlife, has influenced acceptance of the concept that welfare of wild animals is important.

Changes in demographics of wildlife biology and changes in public opinion

The field of fish and wildlife management was initially reductionist, reflecting its initial goals of supporting and managing the consumptive sports of hunting and fishing, and most of the financial support for wildlife management agencies came from the sales of hunting and fishing licenses. Much of the research and management activity on wild animals originated because of the need to regulate, manage, and maintain wild animal populations for hunting and fishing. Nongame species were largely ignored. Most of the people attracted to such careers had backgrounds in hunting and fishing. Initially, such backgrounds somewhat inured biologists to the potential for pain, distress, and suffering of the wild animals that they studied. The social context of wildlife management has changed over the years. Fewer hunting and fishing licenses have been sold annually, forcing agencies to seek support from other sources (Jacobson et al. 2007; Hutchins et al. 2009). Public support for hunting and fishing has decreased as societies have become more urban while public concern and support for animals for nonconsumptive uses has increased (Butler et al. 2003; Jacobson and Decker 2006; Manfredo 2008). The changing human social dimensions of wildlife mean that managers find themselves dealing with multiple opinions, with animal welfare considerations becoming increasingly important (Dubois and Fraser 2013; Dubois and Harshaw 2013).

Appreciation of the increasing complexity of wildlife and management

Fish and wildlife management has largely focused on management of populations whereas animal welfare interests have mainly focused on individual animals. The two approaches are not incompatible if the welfare status of a population of animal populations is considered to be the collective of the welfare status of the individual animals that compose it. With that understanding, expression of judgments of the welfare of a population is a shorthand for the welfare of the individual animals in it, similar to the way a statistical mean is an expression of the central tendency of a population. This view allows for complexities caused by variations in the welfare states of individuals over time and for a range of welfare states of individuals that might occur within the population (Yeates 2013; Beausoleil et al. 2014; Ohl and Putman 2014). This view also places increased importance on the anthropogenic influences on the welfare of individual animals as they are exposed to the manipulations of managers and researchers.

An increasing appreciation for the complexities of life is influencing research and management of wild animals. The scope for variation is enormous when considering when to sample and how to interpret results. There can be variation between individuals and within an individual as well as between populations, sexes, seasons, life history stages, and the procedural and analytical techniques used in a study. Today's scientist must be aware of how the variations due to the complexity of life can influence the data collected and the conclusions drawn in each study.

Chemical immobilization and sedation

In order to allow wildlife science to progress beyond observations and lethal sampling, it was necessary to develop some means of capturing wild animals alive. For animals that are small and harmless to man, netting, trapping, and physical restraint was sufficient. However, for large or dangerous animals, a means of immobilization and restraint that was essentially harmless to the animal and offered safety to the handlers was required. Chemical immobilization of wild animals started in the 1950s by feeding drugs to animals or by coating the drugs on the surface of darts (Hall et al. 1953). Its development has continued apace (Harthoorn 1970; Kock et al. 2012; Jessup et al. 2014). Chemical immobilization has allowed work to be done on a wide variety of animals while reducing the stress on the animals due to handling. The development of improved immobilization equipment, training opportunities, and drugs has improved both the success of capture efforts and the safety of the animals captured. The use of multiple drugs in the immobilization of wild animals has improved safety margins by reducing the concentration of any single drug by targeting multiple types of receptors. The availability of reversal agents has allowed for the manipulation of immobilization times and improved the safety of chemical immobilization. Books on the capture of wild animals include much information about procedures and drugs and are useful resources whenever a new species is to be captured (Nielsen 1999; Kreeger and Arnemo 2012; West et al. 2014).

Monitoring during field immobilization

Since the beginnings of chemical immobilization of wild animals, measurement of body temperature has been the most common monitoring of animal well-being, with observation of respiration and heart rate (although not necessarily measurements thereof) also done. In recent years the development of portable, battery-powered devices has allowed for direct monitoring of the physiologic state of the animal in real-time. Such devices include pulse oximeters for determining oxygen saturation of hemoglobin, heart monitors for rate and rhythm, electrocardiograms, capnographs for exhaled carbon dioxide, point-of-care devices for clinical pathology, and devices to measure a variety of other analytes including blood gases (for reviews, see Plebani and Lippi 2014; Stoot et al. 2014; see also Harms et al., this supplement). Most of these devices were designed for indoor use, and their use for monitoring wild animal captures offers performance challenges in environmental conditions that are sometimes less than ideal (Louie et al. 2014). Such devices have proved useful in studies of capture or immobilization of wild animals including such parameters as positioning (Posner et al. 2005; Radcliffe et al. 2014), oxygen supplementation (Bush et al. 2012; Fahlman et al. 2012; Lian et al. 2014), comparison of capture techniques (Cooke et al. 2008; Pfitzer et al. 2014), and prediction of mortality (Hobbs et al. 2010; Sobhian et al. 2012; Stacy et al. 2013). The further use of such monitoring devices during wildlife capture events should permit a more-refined investigation of the potential effects of capturing, handling, and manipulating wild animals that would be the first steps in developing methods to reduce adverse effects.

Noninvasive sampling

Clearly, animal welfare is advanced if adequate samples can be collected without capturing and handling animals. To that end, noninvasive sampling techniques have been developed using hair, feces, breath, saliva, antlers, feathers, eggs, images (using camera traps), body temperature (via thermal imaging), water (for fish), footprints, shed skin, and urine (Fossi 1994; Keay et al. 2006; Darimont et al. 2008; Meyer and Novak 2012; McCafferty 2013; Gu et al. 2014). Noninvasive sampling techniques need to be tested and validated before the results obtained can be considered to be equivalent to those from traditional samples such as blood and biopsies (Palme 2005; Sheriff et al. 2010). Presently, enough results showing variation and issues with noninvasively-gathered samples exist to urge caution when considering using such samples (Martinsen et al. 2014; Mastromonaco et al. 2014; Mesa-Cruz et al. 2014).

Ongoing and future concerns for wild animal welfare

Common sense and self-interest dictate that an effort to minimize adverse effects of research and management activities be an integral part of every field study, remembering that animal welfare determines data quality. Wildlife project proposals need a description of how they will assess the potential for negative effects on their animals in order to assure the quality of the data to be gathered. Further research to examine the effects of techniques used on wild animals, and to identify missing information on the potential adverse effects, will be an essential part of future improvements in wild animal welfare. Publication of adverse effects, as experienced in both controlled experiments and in field studies, will be valuable contributions to improving wild animal welfare. Also, failures of equipment such as transmitters and data loggers need to be documented and published, as deployment of faulty devices represent unfruitful animal capture and handling. Journal editors need to develop and enforce high standards of animal welfare as reflected in the articles that they select and publish. An increased emphasis can be placed on documenting and reducing morbidity of capture and handling (e.g., stress, distress, fear, pain, infection, inflammation) rather than using actual mortality, a cruder measure of the outcome of the procedures used in wildlife research.

Some specific issues can be identified that are of present or rising concern. For example, the issue of whether or not fish can feel pain is currently being vigorously debated (Rose et al. 2013; Sneddon 2015). The effects of clipping fins (e.g., adipose fins) for marking fish are of growing concern (Roques et al. 2010; Petersson et al. 2014). The effects of catch-and-release angling are being actively investigated, particularly from a physiologic viewpoint (Meka and McCormick 2005; Gale et al. 2011; Cooke et al. 2013a). The effects of handling of fish, and especially of exposure to air, is being determined to be of fundamental importance in the quality and survival of targeted and bycatch species (Raicevich et al. 2014; Rapp et al. 2014). Handling and killing of fish caught during commercial fishing and aquaculture harvest has become an important area of research as aquaculturists have discovered that the quality of their product is directly related to the welfare of their livestock (Lines and Spence 2014; Pettersen et al. 2014; Simitzis et al. 2014). Recently, the necessity of aseptic surgical techniques during the coelomic implantation of transmitters and data loggers into fish has been debated (Mulcahy 2013; Jepsen et al. 2014a, b; Mulcahy 2014; Mulcahy and Harms 2014).

The techniques used to mark wild animals for identification continue to be controversial and an active subject for study, as each technique has advantages and disadvantages as well as proponents and detractors. For amphibians and small mammals, there has been a long controversy over clipping toes as a marking technique, with research showing both the presence and absence of harm to the animals so marked, depending on species, sample size, and statistical technique used (McCarthy and Parris 2004; Parris et al. 2010; Perry et al. 2011). For mammals, concern has been expressed over the possible adverse effects of pulling teeth for aging as well as over the proper use of analgesia during such extractions (Nelson 2002; Mansfield et al. 2006). The techniques used for both lethal- and nonlethal trapping have long been debated, but research is improving understanding of the process (e.g., Warburton et al. 2000; Iossa et al. 2007; Baker and Macdonald 2012; Proulx et al. 2015). Branding of wild animals has been especially controversial, particularly in pinnipeds (e.g., McMahon et al. 2006; Beausoleil and Mellor 2007; McMahon et al. 2007; Wilkinson et al. 2011). That branding is controversial when used on wild animals should not be surprising, as its use on domestic livestock, which stretches back hundreds of years, is still poorly investigated and still attracts criticism and study (e.g., Schwartzkopf-Genswein et al. 1997a, b; Tucker et al. 2014).

Sedation has been used to reduce the stress of handling of large mammals (e.g., Knox et al. 1990; Pang et al. 2006; López-Olvera et al. 2007; Casas-Díaz et al. 2010; Mentaberre et al. 2010; Toosi et al. 2013). Rapid sedation of small animals being captured without chemical immobilization offers them some of the reduction in stress experienced by larger or more-dangerous animals that are captured and handled under a general anesthetic. If a drug with amnesiac qualities (e.g., midazolam) is used, it is possible that the animal will not remember its handling after onset of the action of the drug. The use of sedation to reduce the stresses of capture and handling is being investigated for use in birds and small mammals, (Mans et al. 2012; Sadegh 2013; Heatley et al. 2015). Recently, sedation has been extended to large whales to improve handling for disentanglement efforts (Van Der Hoop et al. 2013; Barratclough et al. 2014). For all taxa, understanding the limits as well as the development and refinement of attachment techniques for tags and electronic devices is a continuing quest (Vandenabeele et al. 2011; Cooke et al. 2013b; Jones et al. 2013).

CONCLUSIONS

The welfare of the animals used in wildlife research is one of the primary determinants of the quality of the data gathered and, hence, the quality of the conclusions and management decisions reached. The attention being paid to evaluate the effects of research and management actions in field studies of free-ranging animals has been receiving increased attention in recent years. It is in the best interests of all stakeholders to expect, consider, and implement improvements in animal welfare in wildlife research. Although wildlife researchers and managers will need to pursue improvements in animal welfare to assure the quality of their work, in the end it will be the opinions of the general public that will judge our efforts in animal welfare.

ACKNOWLEDGMENTS

Dr. Daniel Mulcahy graciously allowed the editorial team to use his 2014 American Association of Wildlife Veterinarians Al Franzmann Award presentation as the inspiration for the introduction to the supplement, and we are indebted to his kindness for doing so.

Supplement Editorial Board

Kevin Castle

Colin Gillin

Sonia Hernandez

Anne Justice-Allen

Nadine Lamberski

Megin Nichols

Peregrine Wolff

LITERATURE CITED

American College of Animal Welfare (ACAW)
2015
.
ACAW Definition of Animal Welfare
. http://www.acaw.org/animal_welfare_principles.html.
Accessed June 2015
.
Baker
SE
,
Macdonald
DW.
2012
.
Not so humane mole tube traps
.
Anim Welfare
21
:
613
615
.
Barratclough
A
,
Jepson
PD
,
Hamilton
PK
,
Miller
CA
,
Wilson
K
,
Moore
MJ.
2014
.
How much does a swimming, underweight, entangled right whale (Eubalaena glacialis) weigh? Calculating the weight at sea to facilitate accurate dosing of sedatives to enable disentanglement
.
Mar Mammal Sci
30
:
1589
1599
.
Beausoleil
NJ
,
Appleby
MC
,
Weary
DM
,
Sandøe
P.
2014
.
Balancing the need for conservation and the welfare of individual animals
. In:
Dilemmas in animal welfare
,
Appleby
MC
,
Veary
DM
,
Sandoe
P
,
editors.
CAB International
,
Oxfordshire, UK
. pp.
124
147
.
Beausoleil
NJ
,
Mellor
DJ.
2007
.
Investigator responsibilities and animal welfare issues raised by hot branding of pinnipeds
.
Aus Vet J
85
:
484
485
.
Bush
M
,
Raath
JP
,
Grobler
D
,
Klein
L.
2012
.
Severe hypoxaemia in field-anaesthetised white rhinoceros (Ceratotherium simum) and effects of using tracheal insufflation of oxygen
.
J S Afr Vet Assoc
75
:
79
84
.
Butler
JS
,
Shanahan
J
,
Decker
DJ.
2003
.
Public attitudes toward wildlife are changing: A trend analysis of New York residents
.
Wildl Soc Bull
31
:
1027
1036
.
Cardon
AD
,
Bailey
MR
,
Bennett
BT.
2012
.
The animal welfare act: From enactment to enforcement
.
J Am Assoc Lab Anim Sci
51
:
301
.
Carey
MJ.
2011
.
Investigator disturbance reduces reproductive success in short-tailed shearwaters Puffinus tenuirostris
.
Ibis
153
:
363
372
.
Casas-Díaz E
,
Marco
I
,
López-Olivera
JR
,
Mentaberre
G
,
Lavín
S.
2010
.
Use of acepromazine for stress control in Spanish ibex (Capra pyrenaica) captured by drive-net
.
Vet J
183
:
332
336
.
Casselman
T.
2006
.
Elizabeth Beard Losey, first female member of the Wildlife Society
.
Wildl Soc Bull
34
:
558
.
Cooke
SJ
,
Donaldson
MR
,
O'Oonnor
CM
,
Raby
GD
,
Arlinghaus
R
,
Danylchuk
AJ
,
Hanson
KC
,
Hinch
SG
,
Clark
TD
,
Patterson
DA.
2013a
.
The physiological consequences of catch-and-release angling: Perspectives on experimental design, interpretation, extrapolation and relevance to stakeholders
.
Fish Manag Ecol
20
:
268
287
.
Cooke
SJ
,
Nguyen
VM
,
Murchie
KJ
,
Thiem
JD
,
Donaldson
MR
,
Hinch
SG
,
Brown
RS
,
Fisk
A.
2013b
.
To tag or not to tag: Animal welfare, conservation, and stakeholder considerations in fish tracking studies that use electronic tags
.
J Intl Wildl Law Pol
16
:
352
374
.
Cooke
SJ
,
Suski
CD
,
Danylchuk
SE
,
Danylchuk
AJ
,
Donaldson
MR
,
Pullen
C
,
Bultê
G
,
O'Toole
A
,
Murchie
KJ
,
Koppelman
JB
,
Shultz AD
,
Brooks
E
,
Goldberg
TL.
2008
.
Effects of different capture techniques on the physiological condition of bonefish Albula vulpes evaluated using field diagnostic tools
.
J Fish Biol
73
:
1351
1375
.
Darimont
CT
,
Reimchen
TE
,
Bryon
H
,
Paquet
P.
2008
.
Faecal-centric approaches to wildlife ecology and conservation; methods, data and ethics
.
Wildl Biol Prac
4
:
73
87
.
Dubois
S
,
Fraser
D.
2013
.
Rating harms to wildlife: A survey showing convergence between conservation and animal welfare views
.
Anim Welfare
22
:
49
55
.
Dubois
S
,
Harshaw
HW.
2013
.
Exploring “humane” dimensions of wildlife
.
Hum Dimen Wildl
18
:
1
19
.
Fahlman
Å
,
Caulkett
N
,
Arnemo
JM
,
Neuhaus
P
,
Ruckstuhl
KE.
2012
.
Efficacy of a portable oxygen concentrator with pulsed delivery for treatment of hypoxemia during anesthesia of wildlife
.
J Zoo Wildl Med
43
:
67
76
.
Fossi
MC.
1994
.
Nondestructive biomarkers in ecotoxicology
.
Environ Health Perspect
102
:
49
54
.
Frank
D.
2013
.
Bad conservation research is unethical conservation research
.
J Bioethic Inq
10
:
539
540
.
Gale
MK
,
Hinch
SG
,
Eliason
EJ
,
Cooke
SJ
,
Patterson
DA.
2011
.
Physiological impairment of adult sockeye salmon in fresh water after simulated capture-and-release across a range of temperatures
.
Fish Res
112
:
85
95
.
Gu
J
,
Alibhai
SK
,
Jewell
ZC
,
Jiang
G
,
Ma
J.
2014
.
Sex determination of Amur tigers (Panthera tigris altaica) from footprints in snow
.
Wildl Soc Bull
38
:
495
502
.
Hall
TC
,
Taft
EB
,
Baker
WH
,
Aub
JC.
1953
.
A preliminary report on the use of flaxedil to produce paralysis in the white-tailed deer (Odocoileus virginianus borealis)
.
J Wildl Manage
17
:
516
520
.
Harthoorn
AM.
1970
.
The flying syringe. Ten years of immobilising wild animals in Africa
.
Geoffrey Bles
,
London, England
,
287
pp.
Heatley
JJ
,
Cary
J
,
Kingsley
L
,
Beaufrere
H
,
Russell
KE
,
Voelker
G.
2015
.
Midazolam sedates Passeriformes for field sampling but affects multiple venous blood analytes
.
Vasc Health Risk Manage
2015
:
61
69
.
Herzog
HA
, Jr,
Betchart
NS
,
Pittman
RB.
1991
.
Gender, sex role orientation, and attitudes toward animals
.
Anthrozoos
4
:
184
191
.
Hobbs
TR
,
O'Malley
JP
,
Khouangsathiene
S
,
Dubay
C.
2010
.
Comparison of lactate, base excess, bicarbonate, and pH as predictors of mortality after severe trauma in Rhesus macaques (Macaca mulatta)
.
Comparative Med
60
:
233
239
.
Hutchins
M
,
Eves
HE
,
Mittermeier
CG
,
Manfredo
MJ
,
Vaske
JJ
,
Brown
P
,
Decker
DJ
,
Duke
EA.
2009
.
Fueling the conservation engine: Where will the money come from to drive fish and wildlife management and conservation?
In:
Wildlife and society: The science of human dimensions
,
Manfredi
MJ
,
Vaske
JJ
,
Brown
PJ
,
Decker
DJ
,
Duke
EA
,
editors.
Island Press
,
Washington, DC
. pp.
184
197
.
Iossa
G
,
Soulsbury
CD
,
Harris
S.
2007
.
Mammal trapping: A review of animal welfare standards of killing and restraining traps
.
Anim Welfare
16
:
335
352
.
Jacobson
CA
,
Decker
DJ.
2006
.
Ensuring the future of state wildlife management: Understanding challenges for institutional change
.
Wildl Soc Bull
34
:
531
536
.
Jacobson
CA
,
Decker
DJ
,
Carpenter
L.
2007
.
Securing alternative funding for wildlife management: Insights from agency leaders
.
J Wildl Manage
71
:
2106
2113
.
Jepsen
N
,
Boutrup
TS
,
Midwood
JD
,
Koed
A.
2014a
.
Fish surgery—A dirty business? Comments to a letter submitted by D
.
Mulcahy and C.A. Harms. Fish Res
156
:
6
8
.
Jepsen
N
,
Cooke
S
,
Aarestrup
K.
2014b
.
Tagging fish in the field: Ethical and procedural considerations
.
J Fish Wildl Manage
5
:
441
444
.
Jessup
DA
,
Dejesus
SR
,
Clark
WE
,
Bleich
VC.
2014
.
Evolution of ungulate capture techniques in California
.
Calif Fish Game
100
:
491
526
.
Jones
TT
,
Van Houtan
KS
,
Bostrom
BL
,
Ostafichuk
P
,
Mikkelsen
J
,
Tezcan
E
,
Carey
M
,
Imlach
B
,
Seminoff
JA.
2013
.
Calculating the ecological impacts of animal-borne instruments on aquatic organisms
.
Methods Ecol Evol
4
:
1178
1186
.
Keay
JM
,
Singh
J
,
Gaunt
MC
,
Kaur
T.
2006
.
Fecal glucocorticoids and their metabolites as indicators of stress in various mammalian species: A literature review
.
J Zoo Wildl Med
37
:
234
244
.
Kellert
SR
,
Berry
JK.
1987
.
Attitudes, knowledge, and behaviors toward wildlife as affected by gender
.
Wildl Soc Bull
15
:
363
371
.
Knox
CM
,
Hattingh
J
,
Raath
JP.
1990
.
The effect of tranquillizers on the immediate responses to repeated capture and handling of boma-kept impala
.
Comp Biochem Phys C
95
:
247
251
.
Kock
MD
,
Lance
WR
,
Jessup
DA.
2012
.
The art of chemical capture: Advances in wildlife capture pharmacology
.
Wildl Prof
6
:
34
39
.
Kreeger
TJ
,
Arnemo
JM.
2012
.
Handbook of wildlife chemical immobilization
.
2nd Ed
.
Published by Author. 448
pp
.
Lian
M
,
Evans
AL
,
Bertelsen
MF
,
Fahlman
Å
,
Haga
HA
,
Ericsson
G
,
Arnemo
JM.
2014
.
Improvement of arterial oxygenation in free-ranging moose (Alces alces) immobilized with etorphine-acepromazine-xylazine
.
Acta Vet Scand
56
:
51
.
Lines
JA
,
Spence
J.
2014
.
Humane harvesting and slaughter of farmed fish
.
Rev Sci Tech OIE
33
:
255
264
.
López-Olvera
JR
,
Marco
I
,
Montané
J
,
Casa-Díaz
E
,
Lavín
S.
2007
.
Effects of acepromazine on the stress response in Southern chamois (Rupicapra pyrenaica) captured by means of drive-nets
.
Can J Vet Res
71
:
41
51
.
Louie
RF
,
Ferguson
WJ
,
Curtis
CM
,
Vy
JH
,
Kost
GJ.
2014
.
Vulnerability of point-of-care test reagents and instruments to environmental stresses: Implications for health professionals and developers
.
Clin Chem Lab Med
52
:
325
335
.
Manfredo
MJ.
2008
.
Who cares about wildlife?
Springer
,
New York
,
236
pp.
Mans
C
,
Guzman
DS-M
,
Lahner
LL
,
Paul-Murphy
J
,
Sladky
KK.
2012
.
Sedation and physiologic response to manual restraint after intranasal administration of midazolam in Hispaniolan Amazon parrots (Amazona ventralis)
.
J Avian Med Surg
26
:
130
139
.
Mansfield
KG
,
Verstraete
FJM
,
Pascoe
PJ.
2006
.
Mitigating pain during tooth extraction from conscious deer
.
Wildl Soc Bull
34
:
201
202
.
Martinsen
ES
,
Brightman
H
,
Fleischer
RC.
2014
.
Fecal samples fail in PCR-based diagnosis of malaria parasite infection in birds
.
Conserv Genet Res
7
:
15
17
.
Mastromonaco
GF
,
Gunn
K
,
McCurdy-Adams
H
,
Edwards
DB
,
Schulte-Hostedde
AI.
2014
.
Validation and use of hair cortisol as a measure of chronic stress in eastern chipmunks (Tamias striatus)
.
Conserv Physiol
2:cou055.
doi:.
McCafferty
DJ.
2013
.
Applications of thermal imaging in avian science
.
Ibis
155
:
4
15
.
McCarthy
MA
,
Parris
KM.
2004
.
Clarifying the effect of toe clipping on frogs with Bayesian statistics
.
J Appl Ecol
41
:
780
786
.
McMahon
CR
,
Bradshaw
CJA
,
Hays
GC.
2006
.
Branding can be justified in vital conservation research
.
Nature
439
:
392
.
McMahon
CR
,
Bradshaw
CJA
,
Hays
GC.
2007
.
Applying the heat to research techniques for species conservation
.
Conserv Biol
21
:
271
273
.
McMahon
CR
,
Hindell
MA
,
Harcourt
RG.
2012
.
Publish or perish: Why it's important to publicise how, and if, research activities affect animals
.
Wildl Res
39
:
375
377
.
Meka
JM
,
McCormick
SD.
2005
.
Physiological response of wild rainbow trout to angling: Impact of angling duration, fish size, body condition, and temperature
.
Fish Res
72
:
311
322
.
Mentaberre
G
,
López-Olvera
JR
,
Casas-Díaz
E
,
Bach-Raich
E
,
Marco
I
,
Lavín
S.
2010
.
Use of haloperidol and azaperone for stress control in roe deer (Capreolus capreolus) captured by means of drive-nets
.
Res Vet Sci
88
:
531
535
.
Mesa-Cruz
JB
,
Brown
JL
,
Kelly
MJ.
2014
.
Effects of natural environmental conditions on faecal glucocorticoid metabolite concentrations in jaguars (Panthera onca) in Belize
.
Conserv Physiol
2
:
cou039.
doi:
Meyer
JS
,
Novak
MA.
2012
.
Minireview: Hair cortisol: A novel biomarker of hypothalamic-pituitary-adrenocortical activity
.
Endocrinology
153
:
4120
4127
.
Mulcahy
DM.
2003
.
Does the Animal Welfare Act apply to free-ranging animals?
ILAR Journal
44
:
252
258
.
Mulcahy
DM.
2013
.
Legal, ethical, and procedural bases for the use of aseptic techniques to implant electronic devices
.
J Fish Wildl Manage
4
:
211
219
.
Mulcahy
DM.
2014
.
A reply to Jepsen, N
.,
K. Aarestrup and S.J. Cooke. Tagging fish in the field: Ethical and procedural considerations. A comment to the recent paper of D. Mulcahy; Legal, ethical and procedural bases for the use of aseptic techniques to implant electronic devices. J Fish Wildl Manage
5
:
445
449
.
Mulcahy
DM
,
Harms
CA.
2014
.
Experimental methods fail to address the questions posed in studies of surgical techniques
.
Fish Res
156
:
1
5
.
Nelson
ME.
2002
.
The science, ethics, and philosophy of tooth extractions from live-captured white-tailed deer: a response to Festa-Bianchet et al. (2002)
.
Wildl Soc Bull
30
:
284
288
.
Nicholson
KL
,
Krausman
PR
,
Merkle
JA.
2008
.
Hypatia and the Leopold standard: Women in the wildlife profession 1937–2006
.
Wildl Biol Pract
4
:
57
72
.
Nielsen
L.
1999
.
Chemical immobilization of wild and exotic animals
.
Iowa State University Press
,
Ames, Iowa
,
342
pp.
Ohl
F
,
Putman
RJ.
2014
.
Animal welfare at the group level: More than the sum of individual welfare?
Acta Biotheor
62
:
35
45
.
Palme
R.
2005
.
Measuring fecal steroids: Guidelines for practical application
.
Ann NY Acad Sci
1046
:
75
80
.
Pang
DSJ
,
Rondenay
Y
,
Measures
L
,
Lair
S.
2006
.
The effect of two dosages of midazolam on short-duration anesthesia in the harp seal (Phoca groenlandica)
.
J Zoo Wildl Med
37
:
27
32
.
Parris
KM
,
McCall
SC
,
McCarthy
MA
,
Minteer
BA
,
Steele
K
,
Bekessy
S
,
Medvecky
F.
2010
.
Assessing ethical trade-offs in ecological field studies
.
J Appl Ecol
47
:
227
234
.
Paul
ES
,
Podberscek
AL.
2000
.
Veterinary education and students' attitudes towards animal welfare
.
Vet Rec
146
:
269
272
.
Perry
G
,
Wallace
MC
,
Perry
D
,
Curzer
H
,
Muhlberger
P.
2011
.
Toe clipping of amphibians and reptiles: Science, ethics, and the law
.
J Herpetol
45
:
547
555
.
Petersson
E
,
Rask
J
,
Ragnarsson
B
,
Karlsson
L
,
Persson
J.
2014
.
Effects of fin-clipping regarding adult return rates in hatchery-reared brown trout
.
Aquaculture
422
423
:
249
252
.
Pettersen
JM
,
Bracke
MBM
,
Midtlyng
PJ
,
Folkedal
O
,
Stien
LH
,
Steffenak
H
,
Kristiansen
TS.
2014
.
Salmon welfare index model 2.0: An extended model for overall welfare assessment of caged Atlantic salmon, based on a review of selected welfare indicators and intended for fish health professionals
.
Rev Aquac
6
:
162
179
.
Pfitzer
S
,
Ganswindt
A
,
Fosgate
GT
,
Botha
PJ
,
Myburgh
JG.
2014
.
Capture of farmed Nile crocodiles (Crocodylus niloticus): Comparison of physiological parameters after manual capture and after capture with electrical stunning
.
Vet Rec
175
:
304
.
Phillips
C
,
Izmirli
S
,
Aldavood
J
,
Alonso
M
,
Choe
B
,
Hanlon
A
,
Handziska
A
,
Illmann
G
,
Keeling L
,
Kennedy
M.
2010
.
An international comparison of female and male students' attitudes to the use of animals
.
Animals
1
:
7
26
.
Plebani
M
,
Lippi
G.
2014
.
Point of care testing: Evolving scenarios and innovative perspectives
.
Clin Chem Lab Med
52
:
309
311
.
Pollard-Williams
S
,
Doyle
RE
,
Freire
R.
2014
.
The influence of workplace learning on attitudes toward animal welfare in veterinary students
.
J Vet Med Educ
41
:
253
257
.
Posner
LP
,
Woodie
JB
,
Curtis
PD
,
Erb
HN
,
Gilbert
R
,
Adams
WA
,
Gleed
RD.
2005
.
Acid-base, blood gas, and physiologic parameters during laparoscopy in the head-down position in white-tailed deer (Odocoileus virginianus)
.
J Zoo Wildl Med
36
:
642
647
.
Proulx
G
,
Rodtka
D
,
Barrett
MW
,
Cattet
M
,
Dekker
D
,
Moffatt
E
,
Powell
RA.
2015
.
Humaneness and selectivity of killing neck snares used to capture canids in Canada: A review
.
Can Wildl Biol Manage
4
:
55
64
.
Radcliffe
RW
,
Morkel
P
,
Jago
M
,
Taft
AA
,
Du Preez
P
,
Miller
MA
,
Candra
D
,
Nydam
DV
,
Barry
JS
,
Gleed
RD.
2014
.
Pulmonary dead space in free-ranging immobilized black rhinoceroses (Diceros bicornis) in Namibia
.
J Zoo Wildl Med
45
:
263
271
.
Raicevich
S
,
Minute
F
,
Finoia
MG
,
Caranfa
F
,
Di Muro
P
,
Scapolan
L
,
Beltramini
M.
2014
.
Synergistic and antagonistic effects of thermal shock, air exposure, and fishing capture on the physiological stress of Squilla mantis (Stomatopoda
).
PLoS One
9
:
e105060
.
Rapp
T
,
Hallermann
J
,
Cooke
SJ
,
Hetz
SK
,
Wuertz
S
,
Arlinghaus
R.
2014
.
Consequences of air exposure on the physiology and behavior of caught-and-released common carp in the laboratory and under natural conditions
.
N Am J Fish Manage
34
:
232
246
.
Roques
JAC
,
Abbink
W
,
Geurds
F
,
Van De Vis
H
,
Flik
G.
2010
.
Tailfin clipping, a painful procedure: Studies on Nile tilapia and common carp
.
Physiol Behav
101
:
533
540
.
Rose
JD
,
Arlinghaus
R
,
Cooke
SJ
,
Diggles
BK
,
Sawynok
W
,
Stevens
ED
,
Wynne
CDL.
2013
.
Can fish really feel pain?
Fish Fisheries
15
:
97
133
.
Sadegh
AB.
2013
.
Comparison of intranasal administration of xylazine, diazepam, and midazolam in budgerigars (Melopsittacus undulatus): Clinical evaluation
.
J Zoo Wildl Med
44
:
241
244
.
Schwartzkopf-Genswein
KS
,
Stookey
JM
,
De Passillé
AM
,
Rushen
J.
1997a
.
Comparison of hot-iron and freeze branding on cortisol levels and pain sensitivity in beef cattle
.
Can J Anim Sci
77
:
369
374
.
Schwartzkopf-Genswein
KS
,
Stookey
JM
,
Janzen
ED
,
McKinnon
J.
1997b
.
Effects of branding on weight gain, antibiotic treatment rates and subsequent handling ease in feedlot cattle
.
Can J Anim Sci
77
:
361
367
.
Sheriff
MJ
,
Krebs
CJ
,
Boonstra
R.
2010
.
Assessing stress in animal populations: Do fecal and plasma glucorticoids tell the same story?
Gen Comp Endocr
166
:
614
619
.
Simitzis
PE
,
Tsopelakos
A
,
Charismiadou
MA
,
Batzina
A
,
Deligeorgis
SG
,
Miliou
H.
2014
.
Comparison of the effects of six stunning/killing procedures on flesh quality of sea bass (Dicentrarchus labrax, Linnaeus 1758) and evaluation of clove oil anaesthesia followed by chilling on ice/water slurry for potential implementation in aquaculture
.
Aquac Res
45
:
1759
1770
.
Sneddon
LU.
2015
.
Pain in aquatic animals
.
J Exp Biol
218
:
967
976
.
Sobhian
B
,
Kröpfl
A
,
Hölzenbein
T
,
Khadem
A
,
Redl
H
,
Bahrami
S.
2012
.
Increased circulating D-lactate levels predict risk of mortality after hemorrhage and surgical trauma in baboons
.
Shock
37
:
473
477
.
Stacy
NI
,
Innis
CJ
,
Hernandez
JA.
2013
.
Development and evaluation of three mortality prediction indices for cold-stunned Kemp's ridley sea turtles (Lepidochelys kempii
).
Conserv Physiol
1
:
cot003
.
Stoot
LJ
,
Cairns
NA
,
Cull
F
,
Taylor
JJ
,
Jeffrey
JD
,
Morin
F
,
Mandelman
JW
,
Clark
TD
,
Cooke
SJ.
2014
.
Use of portable blood physiology point-of-care devices for basic and applied research on vertebrates
.
Conserv Physiol
2
:
cou11
. doi:.
Toosi
BM
,
Gratton
G
,
McCorkell
RB
,
Wynne-Edwards
KE
,
Woodbury
MR
,
Lessard
C.
2013
.
Effects of pipothiazine palmitate on handling stress and on the characteristics of semen collected by electroejaculation in bison (Bison bison) bulls
.
Anim Reprod Sci
138
:
55
63
.
Tucker
CB
,
Mintline
EM
,
Banuelos
J
,
Walker
KA
,
Hoar
B
,
Drake
D
,
Weary
DM.
2014
.
Effect of a cooling gel on pain sensitivity and healing of hot-iron cattle brands
.
J Anim Sci
92
:
5666
5673
.
Van Der Hoop
J
,
Moore
M
,
Fahlman
A
,
Bocconcelli
A
,
George
C
,
Jackson
K
,
Miller
C
,
Morin
D
,
Pitchford
T
,
Rowles
T
,
Smith
J
,
Zoodsma
B.
2013
.
Behavioral impacts of disentanglement of a right whale under sedation and the energetic cost of entanglement
.
Mar Mammal Sci
30
:
282
307
.
Vandenabeele
SP
,
Wilson
RP
,
Grogan
A.
2011
.
Tags on seabirds: How seriously are instrument-induced behaviours considered?
Anim Welfare
20
:
559
571
.
Walker
M
,
Diez-León
M
,
Mason
G.
2014
.
Animal welfare science: Recent publication trends and future research priorities
.
Int J Comp Psychol
27
:
80
100
.
Warburton
B
,
Gregory
NG
,
Morriss
G.
2000
.
Effect of jaw shape in kill-traps on time to loss of palpebral reflexes in brushtail possums
.
J Wildl Dis
36
:
92
96
.
West
G
,
Heard
D
,
Caulkett
N
,
editors.
2014
.
Zoo animal and wildlife immobilization and anesthesia
.
2nd Ed.
Wiley Blackwell
,
Ames, Iowa
,
950
pp.
Wilkinson
IS
,
Chilvers
BL
,
Duignan
PJ
,
Pistorius
PA.
2011
.
An evaluation of hot-iron branding as a permanent marking method for adult New Zealand sea lions, Phocarctos hookeri
.
Wildl Res
38
:
51
60
.
Yeates
JW.
2013
.
Individualism and nonindividualism in the application of nonhuman animal welfare to policy
.
J Appl Anim Welfare Sci
16
:
254
271
.
Zommers
Z
,
Macdonald
DW
,
Johnson
PJ
,
Gillespie
TR.
2013
.
Impact of human activities on chimpanzee ground use and parasitism (Pan troglodytes)
.
Conserv Let
6
:
264
273
.