8
A Perspective on Education in Research Ethics for Entomology Graduate Students Rebecca T. Trout, Carey R. Minteer, Godshen R. Pallipparambil, Roxane M. Magnus, and Robert N. Wiedenmann From early childhood, we are taught right from wrong. As we go through life, becoming accountable for our decisions and actions is a big part of the learning process to understand the norms and standards of conduct. Becoming a scientist mirrors that learning process to understand the norms and standards of conduct in science. Science is generally an open process, and proper conduct is expected of all those involved. Transparent scientific methods, appropriate data collection and analysis, and an honest peer review process are needed for science to advance and build upon previous studies. Furthermore, scientists have a social responsibility for being open and sharing findings through publications and presentations. A high standard of ethics, defined by norms of conduct maintained by scientists, is an essential part of the relationship scientists have with society. The era of "big science" in the United States, which began shortly before World War II, has generated great increases in federal fund ing for scientific research. In FY2010, the U.S. government provided more than $150 billion for research and development (AAAS 2010). The goal for investing taxpayer money in mission-oriented research is to improve the lives of all citizens; thus, the use of public funds for scientific research gives the public a stake in the scientific process. Proper and ethical conduct of science is critical to maintaining the public's financial support and trust of scientists. The public ordinarily holds scientists in high regard and presumes the integrity of science and scientists. When scientific integrity is challenged, the public notices. Several well-publicized cases and al legations of scientific misconduct over the past decade have placed the topic of scientific ethics squarely in front of the public, academics, and policy-makers (DHHS 2001, 2009; Chang 2002; Harris 2008; Basken 2009; Miller 2010). Irresponsible conduct of research can lead to changes in policy and funding, creating broad and long-lasting ramifications. The fabrication of stem-cell data by a South Korean researcher led to a ban by South Korea on stem cell research using human eggs (Snyder and Loring 2006). Even though the papers were retracted (Kennedy 2006) and the scientist was removed from his position, the damage was done. South Korea lifted the ban on using human eggs for stem cell research in 2009, but the scientific community lost valuable research time and credibility because of the actions of just a few people. Recent charges that climate change 198 scientists in England withheld data gave skeptics ammunition to challenge the integrity of climate change researchers everywhere; however, two subsequent investigations cleared the researchers of "deliberate malpractice" (Adam and Eilperin 2010). Although ethical issues in science have become more complex and politicized, scientific misconduct is not a recent phenomenon. In the 1870s, Louis Pasteur allegedly used ideas from his rivals and misrepresented his research methods. Other types of misconduct include hoaxes, such as the "discovery" of the Piltdovvn man in 1912. More insidious are experiments conducted in the name of "public good," such as the Tuskegee Syphilis Study. Each report of misconduct diminishes public trust and weakens scientific integrity. Most scientists maintain high ethical research standards; however, they face challenges during research that can blur the definition of proper conduct. Pressures from regulatory demands and competi tion among colleagues may lead to lcss-than-ethical behaviors (De Vriesetal. 2006). Fanelli's study (2009) included a meta-analysis of 18 surveys that exclusively dealt with misconduct in scientific research. These surveys for researchers were analyzed as two parts: research ethics questions about self and colleagues. When asked about self, 2% of the respon dents agreed to have falsified or fabricated research data; however, 33% reported having either "dropped data points due to gut feelings" or "changed the results due to pressure from funding sources." Even worse, when surveyed about their colleagues, 14% of the scientists reported having observed falsification or fabrication ofdata, and 72% of respondents observed questionable scientific practices. Fanelli's study (2009) focused mainly on the fabrication and falsification of research data, but these behaviors are just two of the types of misconduct. Martinson et al. (2005) found that 38% of mid- career and 28% of early-career scientists surveyed in 2002 reported engaging in one or more of 16 misconduct actions. The scientific process begins with observations that spawn ideas that are tested with experiments and shared with peers and the public in publications; it ultimately leads to the formation of new ideas. Publication allows scientists to share discoveries and to give credit to those who contributed to and invested in the study. Peer- reviewed publication is evidence of scientific credibility, the result ofwhich can be professional advancement, prestige, and subsequent American Entomologist Winter 2010

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APerspective on Educationin Research Ethics for Entomology

Graduate Students

Rebecca T. Trout, Carey R. Minteer, Godshen R. Pallipparambil,

Roxane M. Magnus, and Robert N. Wiedenmann

From early childhood, we are taught right from wrong. As wego through life, becoming accountable for our decisions and

actions is a big part of the learning process to understand thenorms and standards of conduct. Becoming a scientist mirrors that

learning process to understand the norms and standards of conduct

in science. Science is generally an open process, and proper conduct

is expected of all those involved. Transparent scientific methods,appropriate data collection and analysis, and an honest peer review

process are needed for science to advance and build upon previous

studies. Furthermore, scientists have a social responsibility for beingopen and sharing findings through publications and presentations.A high standard of ethics, defined by norms of conduct maintained

by scientists, is an essential part of the relationship scientists have

with society.

The era of "big science" in the United States, which began shortlybefore World War II, has generated great increases in federal funding for scientific research. In FY2010, the U.S. government providedmore than $150 billion for research and development (AAAS 2010).The goal for investing taxpayer money in mission-oriented research

is to improve the lives of all citizens; thus, the use of public funds for

scientific research gives the public a stake in the scientific process.

Proper and ethical conduct of science is critical to maintaining the

public's financial support and trust of scientists.

The public ordinarily holds scientists in high regard and presumes

the integrity of science and scientists. When scientific integrity is

challenged, the public notices. Several well-publicized cases and al

legations of scientific misconduct over the past decade have placed

the topic of scientific ethics squarely in front of the public, academics,and policy-makers (DHHS 2001, 2009; Chang 2002; Harris 2008;

Basken 2009; Miller 2010). Irresponsible conduct of research can

lead to changes in policy and funding, creating broad and long-lastingramifications. The fabrication of stem-cell data by a South Korean

researcher led to a ban by South Korea on stem cell research using

human eggs (Snyder and Loring 2006). Even though the paperswere retracted (Kennedy 2006) and the scientist was removed from

his position, the damage was done. South Korea lifted the ban on

using human eggs for stem cell research in 2009, but the scientific

community lost valuable research time and credibility because of

the actions of just a few people. Recent charges that climate change

198

scientists in England withheld data gave skeptics ammunition to

challenge the integrity of climate change researchers everywhere;

however, two subsequent investigations cleared the researchers of

"deliberate malpractice" (Adam and Eilperin 2010).

Although ethical issues in science have become more complex

and politicized, scientific misconduct is not a recent phenomenon.

In the 1870s, Louis Pasteur allegedly used ideas from his rivals and

misrepresented his research methods. Other types of misconduct

include hoaxes, such as the "discovery" of the Piltdovvn man in 1912.

More insidious are experiments conducted in the name of "public

good," such as the Tuskegee Syphilis Study. Each report of misconduct

diminishes public trust and weakens scientific integrity.

Most scientists maintain high ethical research standards; however,

they face challenges during research that can blur the definition of

proper conduct. Pressures from regulatory demands and competi

tion among colleagues may lead to lcss-than-ethical behaviors (De

Vriesetal. 2006).

Fanelli's study (2009) included a meta-analysis of 18 surveys that

exclusively dealt with misconduct in scientific research. These surveys

for researchers were analyzed as two parts: research ethics questionsabout self and colleagues. When asked about self, 2% of the respondents agreed to have falsified or fabricated research data; however,

33% reported having either "dropped data points due to gut feelings"or "changed the results due to pressure from funding sources." Even

worse, when surveyed about their colleagues, 14% of the scientists

reported having observed falsification or fabrication ofdata, and 72%of respondents observed questionable scientific practices.

Fanelli's study (2009) focused mainly on the fabrication andfalsification of research data, but these behaviors are just two of the

types of misconduct. Martinson et al. (2005) found that 38% of mid-

career and 28% of early-career scientists surveyed in 2002 reported

engaging in one or more of 16 misconduct actions.

The scientific process begins with observations that spawn ideas

that are tested with experiments and shared with peers and thepublic in publications; it ultimately leads to the formation of new

ideas. Publication allows scientists to share discoveries and to givecredit to those who contributed to and invested in the study. Peer-

reviewed publication is evidence of scientific credibility, the result

of which can be professional advancement, prestige, and subsequent

American Entomologist • Winter 2010

Page 2: Character 2

research funding. The importance placed on publishing can lead toinappropriate behavior (Macrina 2005), such as changing the resultsof a study because of pressure from the funding source, selectivelyremoving data from an analysis, or publishing results more than once

(Martinson etal. 2005).

Manuscripts that go through peer review before publication are

scrutinized by reviewers, who assist an editor in deciding the merit

of the study and offer constructive criticism to the author (Macrina2005). Reviewers, however, may also be competitors who could ben

efit from delaying or undermining the publication process. Conflicts

of interest can arise when a researcher uses an assigned position of

power to influence decisions for personal gain.

A survey of 231 editors from Wiley-Blackwell science journalsabout 16 potential ethical issues in their publications indicated that

the editors had a low level of awareness of many ethical guidelines.

Most editors, however, welcomed further education/training, which

suggests that training should be an ongoing educational experience

(Wager etal. 2009).

Scientists continue to learn the workings of the scientific process

and ethical behavior involved with conducting research throughout

their careers, but often the learning begins in graduate school. Stu

dents learn ethical behavior and responsible conduct of research inmany ways. Mentors, advisers, faculty, fellow students, and techni

cians all play a part in the day-to-day accumulation of learned ethical

behaviors. This kind of informal ethics education, however, can lead

to significant gaps in a graduate student's understanding of complex

ethical situations.

• We learn how to collect data, but not necessarily when it is

appropriate to exclude data.• We learn how to write a publication, but not when it is time to

publish the results.

• We learn about the need to report conflicts of interest, but

perhaps not what constitutes a conflict.

The definitions used and the emphasis placed on scientific ethicsvary among disciplines, but the norms of scientific ethical behavior

are universal. Some areas of science, such as stem-cell research or

developing and deploying genetically modified organisms, present

complex ethical issues and an increased need for education about

research ethics.

Many academic programs across the United States have recog

nized the need for more formal ethics education in their curricula; for

example, psychology, public health, sociology, and business (Handels-

man 1986, Folse 1991, Sims and Sims 1991, Coughlin et al. 1999).Business programs at several U.S. colleges and universities haveadded courses on ethics at the undergraduate and MBA levels (Sims

and Sims 1991). Medical and law schools that have already incor

porated ethics education into their programs also have standardsof rules, oaths and codes with which to comply (AMA 2001, Gordon

and Parsi 2002, ABA 2009).

In the United Kingdom, the Quality Assurance Agency (2002)set benchmark statements describing desired characteristics ofhigher education programs and provided guidance for forming and

renovating programs, including the biosciences. Several of thosestatements concern the ethical training of students. Students are

expected to "recognize the moral and ethical issues of investigationsand appreciate the need for ethical standards and professional codesof conduct" and "have some understanding of ethical issues and the

American Entomologist • Volume 56, Number 4

impact on society of advances in the biosciences." Graduates should"be able to construct reasoned arguments to support their position

on the ethical and social impact of advances in the biosciences."Pressure from regulatory and funding agencies in the US has

started to swing the pendulum of change toward training in scientificethics.The National Institutes of Health (NIH) requires newscientific

staff to complete several Web-based ethics training modules within90 days of hire (NIH 2009). The National Science Foundation (NSF)recently began requiring institutions to provide training in the ethical

conduct of research for all persons supported by NSFfunds (Plimpton 2009). Although this training is an important step, the question

remains whether a simple training module or workshop is sufficient

to teach the vast complexity of scientific ethics.Discussion of ethical behavior among students and research men

tors varies among individuals and institutions. Students may realize

"cheating is wrong," yet the ethical questions about data acquisition,

statistical analyses, or representation of the results are rarely discussed. Consequently, some of us may fear making a wrong decision;worse, some of us may not even realize that there is a wrong decision.Kligyte et al. (2008) proposed teaching metacognitive strategies

to resolve ethical dilemmas to improve effectiveness of education

on responsible conduct of research. Although most scient manner,

simple ethics questions persist; however, the answers to many of

these questions are rarely simple.

In this article, we describe a seminar course and discussions about

ethics in research, and a national survey we conducted to help usunderstand the preparation of the next generation of entomological

scientists in the responsible conduct of research. Recognizing that

there are numerous ways to define research ethics, we compiled our

own definition from a variety of sources. We define research ethics

as the normal, acceptable behavior of scientists that promotes suchcharacteristics and behaviors in research as honesty, trust, objectivity,

responsibility, openness, and respect. It is our goal to demonstrate

the need for discussion of research ethics among students and their

advisers, and to encourage departments to engage in similar discus

sions with their students.

Seminar on "Ethical Issues in Research"

In spring 2009, we participated in an interactive graduate semi

nar course, "Ethical Issues in Research," through the Department of

Entomology at the University of Arkansas. The course was designedto educate and prepare us for ethical issues in science. The seminar

included multiple relevant topics and was structured for discus

sion to supplement readings and brief presentations. Each topic

in the seminar could have been expanded into a full course. Time

constraints limited the focus to selected topics and contemporary

issues, some of which included

• Research misconduct, such as falsification, plagiarism, obscuring,and fabrication;

• Rules and ethical codes in academia, government and funding agen

cies, and the need to value them as a 'Hippocratic oath';• Criteria for authorship and contributions to publications, and ethi

cal concerns involving peer review and conflicts of interest;• Data ownership, intellectual property rights, and the benefits and

pitfalls of secrecy;

• Two sensitive ethical issues—research using vertebrates and

genetic manipulation;• Promoting research integrity versus regulating research miscon

duct; and

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• Reporting scientific misconduct, and positives and negatives ofwhistle blowing.

The discussions were aided by presentations from experts in

particular fields (e.g., patents and intellectual property rights), andanecdotes from colleagues who had had negative experiences thatcould have been avoided or resolved more effectively if the affected

parties had been familiar with dispute resolution. The seminar notonly covered current ethical concerns in research, but also ways tounderstand research misconduct, report misconduct to appropriate

authorities, and how to avoid missteps along the way.

Through the class discussions, it became apparent that there isno single perspective for any particular issue. The very definition of"ethical" can change depending on an individual's cultural, educational, and research background. Being involved in science can leadto a different perspective on ethics than what the public may possess.Although controversial topics did not uncover great differences inopinion among students, nuances between being "unethical" and"unprofessional" sparked lively discussion.

The nine graduate students were surveyed both before and afterthe semester. The pre-and post-class surveys were to determinewhether participants changed opinions and actions as a result of

the discussions during the class. Two surveys from the book Scien

tific Integrity (Macrina 2005) were used: Overview and ResearchMisconduct. The Overview survey contained 24 yes-no questions;

11 were about ethical behavior (e.g., have you ever plagiarized thework of others?), and 13 questions asked whether topics had been

discussed among members ofa lab or research group. The survey on

Research Misconduct asked how strongly respondents agreed withstatements about ethical research. Statements ranged from having

an obligation to report witnessed research misconduct to whetherall authors of a paper containing fabricated data should share theblame equally.

At the end of the seminar class, we compared the data from the

pre- and post-class surveys. Both surveys were anonymous, and nodata were linked to any individual. A few minor changes in ethicalbehavior and viewpoints were noted, such as the increase in respon

dents who indicated that they would report violations of scientific

integrity by a coworker (increase from 66 to 89%) or supervisor(increase from 55 to 77%). Mean scores increased (toward strong

agreement) for ethical responsibility to report misconduct, willingness to report misconduct, and for equal blame and equal punishment for coauthors of a paper with fabricated data. Most illustrative

were the increases in respondents who indicated they had discussedtopics of research ethics. Among the 13 topics, the pre-class surveyindicated that an average of 33% students had discussed the topics

among lab members, whereas the average of those questions in the

post-class survey increased to 66%.

The changes in attitudes and behaviors observed among theparticipants in the seminar class and the survey results led us toquestion how well entomology graduate students elsewhere are

prepared inresearchethics.Ourdiscussionsultimatelyledtoa surveyof entomology students across North America.

Many departments have required core classes, but few students

review ethical issues in a formal course. In a question posed to de

partment administrators, we asked if their respective university ordepartment required a graduate level course on research ethics. Of25 responses, 3 reported a graduate school or university requirement, 1 had a departmental requirement, and 21 did not have any

requirement.

200

Ethical Research Survey of Entomology Students

After concluding the seminar course, we created a survey onresearch ethics, mostly adapted from Macrina (2005). Our survey(Table 1) was developed to assess entomology graduate studentsaround North America about the level of preparation or discussionthat graduate education provides and how students view researchethics.

Wedeveloped the concept of "Research Leader" to define any individual who may have influenced the education— and, thus, the surveyresponses—of students. Although we anticipated that a ResearchLeader would be a major faculty adviser or advising committee

member, our definition included department chair, course teacher/teaching assistant, lab supervisor (including postdoc), workshopadviser, academic program coordinator or academic mentor. Once the

concept was defined, we asked respondents to acknowledge whetherthey understood the definition; only respondents who understoodthe Research Leader definition were included in the survey.

The survey had three parts. In the first part, we asked respondents to categorize themselves several ways (e.g., graduate studentor other; years of research experience; authorship of a publishedpaper). The 12 questions in the second section asked whether aspecific subject (e.g., criteria for authorship) had been discussedwith or presented by a Research Leader. The third part of the surveywas used to analyze the importance of the 12 topics covered in thesecond part.

We used Survey Monkey (www.surveymonkey.com) to create the

survey, which allowed us to collect, collate, and analyze responseswhile maintaining anonymity of respondents. Participants were

informed that the survey had been declared exempt by the Institutional Review Board of the University of Arkansas, that there was no

obligation to take the survey, and that taking the survey implied consent. Because the survey was developed to protect the respondent'sidentity, we were prevented from identifying institutional affiliations.While taking the survey, participants were not allowed to go back

to a previously answered section. This design allowed us to survey

experiences first, and then opinions.

We sent the link to the survey via e-mail to the electronic mailinglist of members of the Council of Entomology Department Admin

istrators (CEDA) with the request that CEDA members distribute

the link to entomology graduate students in their departments. To

avoid confounding the data, we asked that the survey be sent only toentomology students in multidisciplinary departments. Although thesurvey link was sent to about 35 department heads, we do not knowhow many departments distributed the survey or which depart

ments had students represented in the data. At the request of a headof a multidisciplinary department, we modified the survey slightlyto allow students in other agricultural disciplines to respond and

identify their discipline. The redistribution of the modified surveywas limited, and the number of respondents was small, preclud

ing quantitative comparison with the responses from entomology

students. As with the survey for entomology graduate students, the

identity and institutional affiliation of the non-entomology respondents were unknown.

The survey was made available on the Survey Monkey Web site for

one month. After the survey was completed, the collected responses

were filtered to include responses from only graduate students.Responses were sorted several ways for analysis: by years of experience, by whether the respondent had experience as an author, bywhether the respondent had taken a course in research ethics, and

American Entomologist • Winter 2010

Page 4: Character 2

Table 1. Survey distributed to graduate students in entomology tounderstand their experience and opinions on research ethics.

Part I. Please answer the following questions.

1. Which of the following best describes your position?a. Grad Student

b. Post doc

c. Facultyd. Staff2. Which of the following best describes your experience in research?a. None

b. < 6 months

c. 1 yeard. 1-2 yearse. 3-4 yearsf. >5 years3. Have you ever been the author of a published paper or abstract?(Yes/

No)4. Have you ever worked with vertebrate animals?(Yes/ No)

5. Have you ever worked with genetic technology?(Yes/ No)

In the following questions "Research leader" refers to anyone of thefollowing - Major faculty adviser or advising committee members,department chair, course teachers/TA, lab/trainee supervisor includingpostdoctoral fellows, workshop advisers, seminar/discussion members,academic program coordinators/specialists, or academic guide/mentor.

Part II: Which of the following topics have been discussed betweenyou and a "Research Leader"?(Yes/ No)

1. Methods for proper record keeping2. Responsible ownership, sharing, and retention of research data3. The importance of collaboration and steps to promote successful col

laborations

4. Principles for responsible use of vertebrate/human subjects5. Importance of honestly reporting what you find6. Criteria for what and when to publish7. Criteria for authorship8. Risks of conflicts of interest

9. Responsibilities of peer reviewers10. Roles and responsibilities of mentors and trainees11. Special ethical concern for research involving genetic technology12. Responsibility and strategies for action after having witnessed research

misconduct

Part III: Please give us your opinion on the following statements.Use the scale below to rank the level of your agreement or disagreement with each of the following statements.

1-Strongly Disagree; 2-Disagree; 3-Neither Agree/Disagree; 4-Agree5-Strongly Agree

1. It is important for the "Research Leader" to review the risks of conflictsof interest with graduate students.

2. It is important for the "Research Leader" to discuss the ownership, sharing, and presentation of research data with their graduate students.

3. It is important for the "Research Leader" to discuss the roles and responsibilities of mentors and trainees with their students.

4. Criteria for publishing in peer reviewed journals should be discussed bythe "Research Leader" with graduate students.

5. The "Research Leader" should discuss with graduate students the importance of honestly reporting results in scientific research.

6. The "Research Leader" needs to discuss criteria for authorship with theirgraduate students.

7. The "Research Leader" should discuss data collection and record keepingwith graduate students.

8. Graduate students need to be educated about the responsibilities of apeer reviewer by their "Research Leader".

9. The "Research Leader" should discuss the importance of collaborationsin science with graduate students.

10. The education graduate students receive from their "Research Leader"needs to include the responsibilities and course of action after havingwitnessed research misconduct

11. The "Research Leader" should discuss current ethical concerns about

research with vertebrates/humans with graduate students.12. With research involving genetic technology, the "Research Leader" should

examine and discuss special ethical concerns with graduate students.

American Entomologist • Volume 56, Number 4

by those with specialized research experience (genetic technology,

work with vertebrates).

Results and Discussion of the Survey

The surveyyielded 160 responses, ofwhich 150 were from graduate

students. Responses from two students who had no research experi

ence were removed. Not everyone answered every question, giving

slightly different numbers of responses among questions. Respondentswho did not understand die definition of Research Leader were elimi

nated from the second and third part of the survey, giving us 135 as

the total number of analyzed responses. We combined the responsecategories "Agree"and "Strongly Agree" and counted them as positiveresponses; the categories "Strongly Disagree" and "Disagree" were

counted as negative responses. Responses of "Neither Agree nor

Disagree" were omitted in the positive or negative analyses, but were

included in the total to calculate the percentages.

Discussion on 10ofthe 12 topics (questions on vertebrates and genetictechnology are presented separately) with a Research Leader ranged froma high of85% (honestly reporting results) to a low of29% (taking actions

after witnessing research misconduct), with an overall average of 61%(Fig. I). Only two of the topics were discussed with Research Leaders

by >70% of students. Although only an average of 61% of respondentsdiscussed the 10 topics with their Research Leaders, the importance ofdiscussing the topics averaged 90% (>80% agreed or strongly agreedfor all 10 topics).

Approximately two-thirds ofthe students responded that their research

leader discussed methods for proper record keeping (68%); responsibledata ownership, sharing and retaining research data (64%); or the im

portance of collaborations {15%). In a profession where our data arc-

valued and have implications in industry or the Held, only 45% of the

students responded that they had discussed risks ofconflicts of interest,

and only 29% had discussed responsibilities and actions after witness

ing research misconduct (e.g.. reporting to an ombudsperson or other

authority). In contrast, 85% of the students reported they had discussed

the importance of honestly reporting results. However, 1 respondent(0.7%) did not think discussion about honestly reporting results

was important and 11 respondents (8.2%) were indifferent (neither

agreed or disagreed).We grouped research experience into three categories to cor

relate with beginning students (<1 yr, n = 26), master and doctoral

students (1-4 yr, n = 62), and finishing doctoral candidates (>5 yr, n

= 47) (Fig. 2). The level of discussions did not increase throughout

a student's academic career for all topics. For example, we looked at

the components of publishing and research ethics.

Students with more years of research experience were more likely

to publish and discuss critical components of the publication process

such as authorship and publication criteria; however, discussion of

some of these topics did not increase with experience (Fig. 2). We

were surprised to learn that 19% of students with <1 yr experience

had published a paper. The survey question did not ask about primary

authorship or peer-reviewed publications, and this might explain

the unexpected high percentage. Although 91% of students with >5yr of research experience had a publication record, students with

<1 yr of research experience had comparable levels of discussions

about proper record keeping (69%) and responsibilities of peer

reviewers (69%) as had students with >5 yr of experience (62% for

both categories) (Fig. 2). We did not expect this result; it may have

occurred because research leaders believe that the students with

more experience already have had this discussion or are familiar

201

Page 5: Character 2

100

Topic in Research Ethics

with the topic (many Ph.D. students have already completed a M.Sdegree) and further discussion is not needed for late-stage graduate

students. This result also points out that discussing these subjects is

likely to occur in the initial stages of graduate study.

Students at different levels of research experience did not obvi

ously differ in discussions about specific categories such as record

keeping, conflict of interest, honest reporting of results, and the

responsibilities of peer reviewers. There were differences between

beginning students compared with those with >5 yr of experience

in discussions on criteria for authorship (27% difference), criteria

for publishing (21% difference), actions of witnessing research

misconduct (17% difference), and data ownership (16% difference)

(Fig. 2). Discussion on the importance of collaborations was highest

among those students identifying themselves with 1-4 yr of experi-

IS)

I

0

ra

100 i 1 - 4 years • > 5 years

• Discussed with Research leader

!Importance of discussion

Figure 1. Percentpositive responsesabout whether

discussions about

specific topicsoccurred with

research leaders

and the importanceof those discussions.

Positive responsesabout discussions

were "yes" responses;positive responses forimportance were both"agree and stronglyagree" responses.

ence (82%), compared with those with <1 yr (65%) and those with

>5 yr (72%) experience. It may have been too early in the process

for students with <1 yr of experience to discuss collaborations, and

it may be assumed that students with the most experience already

know the importance.Although there was not an obvious relationship between experi

ence and discussion, the perceived importance of discussion clearly

increased with experience. The overall average response for theimportance of discussion of topics ranged from 87% for those with<1 yr experience, to 89% for those with 1-4 yr of experience, to 93%

for those with 25 yr of experience (Table 2), and positive responsesfor nearly every category increased with experience.

Entomologists often work in disciplines that present different

ethical considerations. Conducting research with genetic technol

ogy (such as breeding transgenic crops)and working with vertebrate animals andhumans (such as medical and veterinary

entomologists) have unique ethical issues.

We asked students about their experience in these research areas and filtered out

the responses from students who did not

work in the two areas. Sixty-nine students

(51%) responded that they worked withgenetic technology. Although 65% (45/69)

of students working with genetic technologybelieved that discussion with the research

leader about special ethical concerns was

important, only 28% (19/69) of the students

reported having discussions with a research

leader. Thirty-four of the students surveyed(25%) responded that they worked with

vertebrate animals. Whereas 53% (17/32,

2 students skipped question) of students

working with vertebrates reported havinga discussion with their research leader on

the responsible use of vertebrate and hu

man subjects, 65% (22/34) of these same

ffi

Isz

Data Ownership Authorship Criteria Publishing Criteria Peer Review

e 100 n

u

|2"OCDifl!/>3O

Q

Record Keeping Honest Reporting Conflicts of Interest ReportingMisconduct

Figure 2. Percent positive responses about discussing various components of publication andresearch for students with different levels of research experience.

202 American Entomologist • Winter 2010

Page 6: Character 2

Table 2. Percent positive responses about the importance ofdiscussing ethical topics among students with different levels ofresearch experience.

% of Positive Responses (n)

Survey topic <lyr(26) l-4yr(62) >5 yr (47)

Honest Reporting 89 89 96

Collaborations 89 89 92

Record Keeping 92 95 98

Peer Review 77 85 87

Data Ownership 96 93 98

Publishing Criteria 89 92 96

Authorship Criteria 100 97 98

Mentor & Trainee 81 84 85

Conflicts of Interest 73 85 92

Reporting Misconduct 81 80 89

Average % positive 87 89 93

responses

students agreed that this discussion is important. The percentagesof positive responses are of concern because universities require

these discussions and have animal care and committee review

boards if vertebrates are used in the laboratory. In addition, laws

(e.g., Animal Welfare Act...1966; Animal Welfare Act...1970; FoodSecurity Act. ..1985) regulate animal welfare in research, and granting

agencies have additional requirements for research with vertebrates.

Although universities and funding agencies do not require ethicaldiscussions ofgenetic technology, they do require training modules ordiscussions on vertebrate use. The data indicated students believed

that these special topics were important to discuss.We also compared responses from students who had enrolled in

an ethics course and those students who had not (Fig. 3). Only 31%

(41/133, 2 skipped this question) of the students surveyed hadenrolled in a course on ethics (12%, <1 yr of research experience;

54%, 1-4 yr; 34%, >5 yr). We expected students who had had an

ethics course to have had more discussions on different topics than

those without the ethics course. With two exceptions (peer review

and conflicts of interest), the positive responses from those students

who had taken an ethics course were greater than those who had not,

but the differences were mostly minor (~5%). Two topics showed

greater differences. Students who had enrolled in an ethics coursehad more discussions on the importance of collaborations (22%difference) and the responsibilities and strategies after witnessing

research misconduct (15% difference). Both cohorts agreed that

discussion of each ethical topic was important. We noted that 100%

of graduate students who had <1 yr research experience and hadtaken an ethics course had discussed honest reporting of data and

collaborations (increases of 20 and 43%, respectively) from beginning students who had not taken an ethics class (data not shown).

Although most differences were minor, ranging from 3 to 10%, more

students with an ethics education class realized the importance of

discussions about research ethics (data not shown).

We were concerned with the few obvious differences in responses

between the two cohorts, but we also recognized that the responses

may have included formal coursework and on-line training modules.Our survey did not ask about the contents of the ethics course. An

online course would generate little discussion. Similarly, a course

offered to a large general audience might address only specific topics

(e.g., plagiarism) and not topics such as conflict of interests, which

can have variable perspectives.

Responsible conduct of research is a crucial challenge for graduate students and researchers throughout the scientific community.

From our survey, we learned that many graduate students are notdiscussing ethical issues with their research leaders; this, too, is notunique to entomology. Several disciplines, however, are adopting fully

developed courses, seminar series, or workshops to provide ethicseducation and create awareness among students about current issues

in research ethics. With this research, we, too, hope to see a campaign

to address the ethical concerns affecting our profession.

Different cultural backgrounds and previous educational or research

experiences of some students may have influenced their perceptions

of a few survey questions. For example, the percentage of respondents

who reported discussions with their research leaders could have

varied based on the students' research experience, especially when aresearch leader expects an experienced student to be well versed inresearch ethics. Another possible explanation for survey results could

include the student's perspective of a

research leader. Even though we defined

"Research Leader" in the survey, it is

possible that students considered only

their advisers to be a research leader.

Students also may have considered the

degree of discussion involved and given

negative scores for what they consid

ered to be insufficient discussions.

We believe that actual discussion

on particular topics is important andoffers greater benefits than on-line

training modules. We also believe thatour survey showed that there are key

topics that need to be discussed—andthat students want to discuss. The

survey results pertaining to conflicts

ofinterestand actions after witnessing

misconduct were troubling; students

responded that they did not have

sufficient discussion on these topics.

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Figure 3. Percent positive responses about discussion with research leaders for students that hadenrolled in an ethics course versus those that had not enrolled in an ethics course.

American Entomologist • Volume 56, Number 4 203

Page 7: Character 2

Similarly, it is necessary to focus on those topics that may be assumedto be known or to have been covered, such as honestly reporting

results and proper recordkeeping, because these topics are vitaltoward scientific integrity.

Conclusions

We believe it is important to recognize a disconnect between

the need for ethical conduct in research and the preparation that

the next generation of entomologists (and other scientists) receive.

Given what we learned in the seminar course and in our analysis of

the survey results, we suggest that more education and discussion

about ethical research are needed. We believe that colleges and

universities need to move beyond identifying the problem and work

toward solutions to prevent research misconduct, rather than rely

on punishment for ethical breaches.

Tutorials are a start and meet agency or regulatory require

ments, but the survey results and our class sessions pointed outthat discussion about topics are more instructive and can result inbetter decision-making. Student participation, using actual examples,

would make the issues more relevant and point out the differencesbetween universal norms and cases that have multiple perspectives.

Small-group discussions benefit from guest speakers with particular

expertise. We benefited from a session with an expert on intellectual

property rights; we would have benefited from a discussion with thecampus ombudsperson, who could have addressed authoritativelytopics such as whistleblowing or consequences of misconduct.

Can ethical behavior be taught in a formal course? Ethical behavior

might be taught, but at least explicit presentation and discussion of

issues would increase awareness about the complexity of issues. Who

should teach an ethics course? Some faculty members may think that

this is not their responsibility, but we believe that educating studentsin ethical research is someone's—maybe everyone's—responsibility.

Should such a course be required? If so, who requires the course—a

department, a graduate school, or a funding agency? Many curricula

are already filled with required courses, so where does one more fit

into a graduate program? What topics should such a course contain?

Responsible conduct of research and the norms of ethical behavior

must be covered in depth, but what about special topics or special

ized areas? We realize that courses in ethics are not designed to

improve the moral fiber of students, but we believe that courses in

ethics should teach skills that allow students to address and resolve

ethical questions in their own research. We believe that it is the

responsibility of our scientific discipline to maintain establishedhigh ethical standards in the scientific community through proper

education and communication.

We all—scientists and citizens alike—benefit from rigorous sci

ence that is conducted responsibly. Our credibility as researchers

will help protect the esteem with which scientists are held by thepublic—the same public who determine funding from federal agen

cies. Although we need to ensure scientific misconduct is brought

to light and punished, it is even more critical to prevent misconductfrom happening. Preventing lapses in ethical behavior, we believe,requires awareness of and discussion about a variety of topics inresearch ethics. Some topics and positions are sacred (e.g., proper

care of vertebrates used in research), whereas other topics are

more subjective (e.g., the importance of collaboration). Awareness

of responsible conduct of research and its importance is vital for thefuture ofentomology and is the responsibilityofallofus. ^jjf

204

Acknowledgments

We thank Josh Hannam and Justin Whitaker for help with sur

vey development and generating ideas during the early stages of

this manuscript, and to the other students who participated in theseminar course. We thank all the students who chose to participate

in the survey and the CEDA members who distributed the survey. Tim

Kring and Randy Luttrell reviewed the manuscript and made helpfulcomments. We also acknowledge support from the Department of

Entomology at the University of Arkansas.

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Rebecca Trout recently finished hei Ph.D. in the Department of Entomologyat the University of Arkansas, and is currently a Post-doc at UC Davis. Herdissertation research focused on the spatial identification and geneticcharacterization of ticks and their relationship with Borrelia and Rickettsiaspecies in Arkansas. Carey Minteer is a Ph.D. student in the Department ofEntomology at the University of Arkansas. Her research focuses on biologicalcontrol of invasive weeds. Godshen Pallipparambil is a Ph.D.student in theDepartment of Entomology at University of Arkansas. His research focuseson the interactions of R-gene mediated resistance in tomato with potatoaphids and omnivorous predators. Roxane M. Magnus is a M.S. student inthe Department of Entomology at the University of Arkansas. Her researchfocuses on the genetic variation of honey bees from the south central andcentral United States. Robert N. Wiedenmann ([email protected]) is the

Head of the Department of Entomology at the University of Arkansas. Hisinterests include invasive species, biological control and bioenergy policy.

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American Entomologist • Volume 56, Number 4 205