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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.

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

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

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

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
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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 of data, 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 midcareer 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. Peerreviewed publication is evidence of scientific credibility, the result of which can be professional advancement, prestige, and subsequent
American Entomologist Winter 2010

research funding. The importance placed on publishing can lead to inappropriate behavior (Macrina 2005), such as changing the results of a study because of pressure from the funding source, selectively removing data from an analysis, or publishing results more than once
(Martinson etal. 2005).

impact on society of advances in the biosciences." Graduates should


"be able to construct reasoned arguments to support their position

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 (Macrina 2005). 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 journals about 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 in many 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

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 scientific ethics.The National Institutes of Health (NIH) requires newscientific staff to complete several Web-based ethics training modules within 90 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 NSF funds (Plimp ton 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 dis cussed. 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

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


ethical situations.

ethics in research, and a national survey we conducted to help us understand 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

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

as the normal, acceptable behavior of scientists that promotes such characteristics 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.

perhaps not what constitutes a conflict.

The definitions used and the emphasis placed on scientific ethics


vary among disciplines, but the norms of scientific ethical behavior
are universal. Some areas of science, such as stem-cell research or

Seminar on "Ethical Issues in Research"

developing and deploying genetically modified organisms, present

complex ethical issues and an increased need for education about


research ethics.

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 designed


to 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

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 have added 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 standards of 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 of higher education programs and provided guidance for forming and renovating programs, including the biosciences. Several of those statements concern the ethical training of students. Students are expected to "recognize the moral and ethical issues of investigations and appreciate the need for ethical standards and professional codes of conduct" and "have some understanding of ethical issues and the
American Entomologist Volume 56, Number 4

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 issuesresearch 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 of


whistle blowing. The discussions were aided by presentations from experts in

Ethical Research Survey of Entomology Students

particular fields (e.g., patents and intellectual property rights), and anecdotes from colleagues who had had negative experiences that could have been avoided or resolved more effectively if the affected parties had been familiar with dispute resolution. The seminar not only covered current ethical concerns in research, but also ways to
understand research misconduct, report misconduct to appropriate

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

authorities, and how to avoid missteps along the way.

Through the class discussions, it became apparent that there is no single perspective for any particular issue. The very definition of "ethical" can change depending on an individual's cultural, educa tional, and research background. Being involved in science can lead to a different perspective on ethics than what the public may possess. Although controversial topics did not uncover great differences in opinion among students, nuances between being "unethical" and
"unprofessional" sparked lively discussion.

The nine graduate students were surveyed both before and after the semester. The pre-and post-class surveys were to determine whether 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 Research Misconduct. The Overview survey contained 24 yes-no questions; 11 were about ethical behavior (e.g., have you ever plagiarized the work of others?), and 13 questions asked whether topics had been discussed among members of a lab or research group. The survey on Research Misconduct asked how strongly respondents agreed with statements about ethical research. Statements ranged from having an obligation to report witnessed research misconduct to whether all authors of a paper containing fabricated data should share the
blame equally. At the end of the seminar class, we compared the data from the

pre- and post-class surveys. Both surveys were anonymous, and no data were linked to any individual. A few minor changes in ethical behavior 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, willing ness to report misconduct, and for equal blame and equal punish ment for coauthors of a paper with fabricated data. Most illustrative were the increases in respondents who indicated they had discussed topics of research ethics. Among the 13 topics, the pre-class survey indicated 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 the participants in the seminar class and the survey results led us to question how well entomology graduate students elsewhere are

We developed the concept of "Research Leader" to define any indi vidual who may have influenced the education and, thus, the survey responsesof students. Although we anticipated that a Research Leader would be a major faculty adviser or advising committee member, our definition included department chair, course teacher/ teaching assistant, lab supervisor (including postdoc), workshop adviser, academic program coordinator or academic mentor. Once the concept was defined, we asked respondents to acknowledge whether they understood the definition; only respondents who understood the Research Leader definition were included in the survey. The survey had three parts. In the first part, we asked respon dents to categorize themselves several ways (e.g., graduate student or other; years of research experience; authorship of a published paper). The 12 questions in the second section asked whether a specific subject (e.g., criteria for authorship) had been discussed with or presented by a Research Leader. The third part of the survey was used to analyze the importance of the 12 topics covered in the second part. We used Survey Monkey (www.surveymonkey.com) to create the survey, which allowed us to collect, collate, and analyze responses while maintaining anonymity of respondents. Participants were informed that the survey had been declared exempt by the Institu tional Review Board of the University of Arkansas, that there was no obligation to take the survey, and that taking the survey implied con sent. Because the survey was developed to protect the respondent's identity, 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 mailing list 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 to entomology students in multidisciplinary departments. Although the survey link was sent to about 35 department heads, we do not know how many departments distributed the survey or which depart ments had students represented in the data. At the request of a head of a multidisciplinary department, we modified the survey slightly to allow students in other agricultural disciplines to respond and identify their discipline. The redistribution of the modified survey
was limited, and the number of respondents was small, preclud

ing quantitative comparison with the responses from entomology

prepared in research ethics.Ourdiscussions ultimatelyledto a survey


of 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 or

students. As with the survey for entomology graduate students, the identity and institutional affiliation of the non-entomology respon
dents were unknown.

department required a graduate level course on research ethics. Of 25 responses, 3 reported a graduate school or university require
ment, 1 had a departmental requirement, and 21 did not have any
requirement.
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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 expe rience, by whether the respondent had experience as an author, by whether the respondent had taken a course in research ethics, and
American Entomologist Winter 2010

Table 1. Survey distributed to graduate students in entomology to understand their experience and opinions on research ethics. Part I. Please answer the following questions.

by those with specialized research experience (genetic technology, work with vertebrates).
Results and Discussion of the Survey

1. Which of the following best describes your position?


a. b. Grad Student Post doc

c.
d.
a.

Faculty
Staff
None

The survey yielded 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

2. Which of the following best describes your experience in research?


b. < 6 months

slightly different numbers of responses among questions. Respondents


who did not understand die definition of Research Leader were elimi

c. e. f.

1 year

d. 1-2 years 3-4 years >5 years 3. 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)

nated from the second and third part of the survey, giving us 135 as the total number of analyzed responses. We combined the response categories "Agree"and "Strongly Agree" and counted them as positive responses; 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.

In the following questions "Research leader" refers to anyone of the following - Major faculty adviser or advising committee members, department chair, course teachers/TA, lab/trainee supervisor including postdoctoral fellows, workshop advisers, seminar/discussion members, academic program coordinators/specialists, or academic guide/mentor.
Part II: Which of the following topics have been discussed between you and a "Research Leader"?(Yes/ No) 1. Methods for proper record keeping 2. Responsible ownership, sharing, and retention of research data 3. The importance of collaboration and steps to promote successful col
laborations

4. 5. 6. 7.
8.

Principles for responsible use of vertebrate/human subjects Importance of honestly reporting what you find Criteria for what and when to publish Criteria for authorship
Risks of conflicts of interest

9. Responsibilities of peer reviewers

10. Roles and responsibilities of mentors and trainees 11. Special ethical concern for research involving genetic technology 12. 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 disagree ment with each of the following statements.
1-Strongly Disagree; 2-Disagree; 3-Neither Agree/Disagree; 4-Agree 5-Strongly Agree

Discussion on 10ofthe 12 topics (questions on vertebrates and genetic technology are presented separately) with a Research Leader ranged from a high of 85% (honestly reporting results) to a low of 29% (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 respondents discussed the 10 topics with their Research Leaders, the importance of discussing the topics averaged 90% (>80% agreed or strongly agreed for all 10 topics). Approximately two-thirds ofthe students responded that their research leader discussed methods for proper record keeping (68%); responsible data ownership, sharing and retaining research data (64%); or the im portance of collaborations {15%). In a profession where our data arcvalued and have implications in industry or the Held, only 45% of the students responded that they had discussed risks of conflicts 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

1. It is important for the "Research Leader" to review the risks of conflicts of interest with graduate students. 2. It is important for the "Research Leader" to discuss the ownership, shar ing, and presentation of research data with their graduate students. 3. It is important for the "Research Leader" to discuss the roles and respon
sibilities of mentors and trainees with their students.

4. Criteria for publishing in peer reviewed journals should be discussed by the "Research Leader" with graduate students. 5. The "Research Leader" should discuss with graduate students the impor tance of honestly reporting results in scientific research. 6. The "Research Leader" needs to discuss criteria for authorship with their graduate students. 7. The "Research Leader" should discuss data collection and record keeping with graduate students. 8. Graduate students need to be educated about the responsibilities of a peer reviewer by their "Research Leader". 9. The "Research Leader" should discuss the importance of collaborations in science with graduate students. 10. The education graduate students receive from their "Research Leader" needs to include the responsibilities and course of action after having
witnessed research misconduct

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 >5
yr of research experience had a publication record, students with <1 yr of research experience had comparable levels of discussions

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.

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


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American Entomologist Volume 56, Number 4

Discussed with Research leader 100

!Importance of discussion
Figure 1. Percent positive responses
about whether discussions about

specific topics
occurred with research leaders

and the importance


of those discussions.

Positive responses
about discussions

were "yes" responses; positive responses for importance were both "agree and strongly

agree" responses.

Topic in Research Ethics


with the topic (many Ph.D. students have already completed a M.S
degree) 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 experi100 i

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

1 - 4 years

> 5 years

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 the importance 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 responses for 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 and
humans (such as medical and veterinary entomologists) have unique ethical issues.

I
0

IS)

We asked students about their experi


ra

ence 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 with


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sz

genetic technology. Although 65% (45/69)


Data Ownership
100 n

Authorship Criteria Publishing Criteria

Peer Review

of students working with genetic technology


believed that discussion with the research

e
u

leader about special ethical concerns was

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"O
CD ifl !/> 3 O

Record Keeping

Honest Reporting Conflicts of Interest

Reporting
Misconduct

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 having
a discussion with their research leader on

Figure 2. Percent positive responses about discussing various components of publication and research for students with different levels of research experience.
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the responsible use of vertebrate and hu

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


American Entomologist Winter 2010

Table 2. Percent positive responses about the importance of

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

discussing ethical topics among students with different levels of research experience.
% of Positive Responses (n) Survey topic Honest Reporting
Collaborations

but the differences were mostly minor (~5%). Two topics showed greater differences. Students who had enrolled in an ethics course had more discussions on the importance of collaborations (22%
difference) and the responsibilities and strategies after witnessing

<lyr(26)
89 89 92 77 96

l-4yr(62)
89

>5 yr (47)
96

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


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

89
95 85 93 92

92 98 87 98
96 98 85 92 89 93

Record Keeping
Peer Review

of graduate students who had <1 yr research experience and had


taken an ethics course had discussed honest reporting of data and collaborations (increases of 20 and 43%, respectively) from begin ning 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).

Data Ownership Publishing Criteria Authorship Criteria


Mentor & Trainee

89 100
81

97
84 85

Conflicts of Interest

73 81 87

Reporting Misconduct
Average % positive
responses

80
89

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

students agreed that this discussion is important. The percentages of 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; Food Security 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 ethical discussions of genetic technology, they do require training modules or
discussions on vertebrate use. The data indicated students believed

(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 gradu
ate students and researchers throughout the scientific community.

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 had enrolled 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
o Students with Ethics Course

From our survey, we learned that many graduate students are not discussing ethical issues with their research leaders; this, too, is not unique to entomology. Several disciplines, however, are adopting fully developed courses, seminar series, or workshops to provide ethics education 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 a research leader expects an experienced student to be well versed in research ethics. Another possible explanation for survey results could
include the student's perspective of a

I Students without Ethics Course

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.

X-

100 i
90

<D

80 70 -

-J
SZ

60
50 40 30 20 10
0

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

ra

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a. o

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Topic in Research Ethics

on particular topics is important and offers greater benefits than on-line training modules. We also believe that our survey showed that there are key topics that need to be discussedand
that students want to discuss. The

survey results pertaining to conflicts ofinterestand actions after witnessing

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

misconduct were troubling; students responded that they did not have sufficient discussion on these topics.
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American Entomologist Volume 56, Number 4

Similarly, it is necessary to focus on those topics that may be assumed


to be known or to have been covered, such as honestly reporting

Acknowledgments We thank Josh Hannam and Justin Whitaker for help with sur

results and proper recordkeeping, because these topics are vital


toward 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

vey development and generating ideas during the early stages of this manuscript, and to the other students who participated in the seminar 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 helpful comments. We also acknowledge support from the Department of Entomology at the University of Arkansas.
References Cited

AAAS. 2010. R&D in the FY 2010 Budget by Agency, http://www.aaas. org/spp/rd/fy2010/totall0c.pdf. ABA. 2009. Center for professional responsibility: Model rules of profes sional conduct, http://www.abanet.org/cpr/mrpc/mrpc_toc.html.
AMA. 2001. Code of medical ethics of the American Medical Association.

ments, but the survey results and our class sessions pointed out that discussion about topics are more instructive and can result in better decision-making. Student participation, using actual examples, would make the issues more relevant and point out the differences between 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 the campus ombudsperson, who could have addressed authoritatively topics 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

ht.tp;//www.ama-assii..o.rg/a_ma/pub/physician-!'esource ethics/code-medical-ethics.shtml.

Animal Welfare Act of 1966. Pub. L, Nprf 9-544 fAugust 24 I9,$$k


Animal Welfare Act Amendments of 1970. Pub. L No. 91-579 (December

24, 1970). Adam, K., and J. Eilperin. 2010. Academic experts clear scientists in 'climate-gate.' Washington Post, http://www.washingtonpost.com/wpdyn/content/article/2010/04/14/AR2010041404001.html. Basken, P. 2009. Science ethics rules leave room for scandals, critics fear. The Chronicle of Higher Education. htlp://chronicle.cpm/article/Science-Ethics-Rules-Leave-/47083/. Chang, K. 2002. On scientific fakery and the systems to catch it. New York Times, http://www.nytimes.com/2002/10/15/science/on-scientificfakery-and-the-systems-to-catch-it.html?pagewanted=l. Coughlin, S. S., W. H, Katz, D. R. Mattison, and A. S. P. H. E. Comm. 1999. Ethics instruction at schools of public health in the United States. Am.
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this is not their responsibility, but we believe that educating students in ethical research is someone'smaybe everyone'sresponsibility. Should such a course be required? If so, who requires the coursea 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

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

responsibility of our scientific discipline to maintain established high ethical standards in the scientific community through proper
education and communication.

We allscientists and citizens alikebenefit from rigorous sci ence that is conducted responsibly. Our credibility as researchers will help protect the esteem with which scientists are held by the publicthe same public who determine funding from federal agen cies. Although we need to ensure scientific misconduct is brought

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Kennedy. D. 2006. Responding tjjfraud. Science 314:1353-1353.


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to light and punished, it is even more critical to prevent misconduct from happening. Preventing lapses in ethical behavior, we believe, requires awareness of and discussion about a variety of topics in research 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 the

future ofentomology and is the responsibilityofall of us.

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ing badly. Nature 435: 737-738. Miller, J. 2010. Professor cleared of scientific misconduct. Salt Lake Tribune. http://www.sltrib.com/news/ci_14122933. NIH. 2009. New Employee Ethics Orientation, http://ethics.od.nih.gov/ newempintro.htm. ,

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Plimpton, S. H. 2009. Responsible conduct of research. National Science Foundation. http://edocket.access.gpo.gov/2009/pdf/E9-19930.pdf. QAA. 2002. Bioscience Subject Benchmark Statements http://www.qaa.ac.uk/

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Sims, R. R., and S. j. Sims. 1991. Increasing applied business ethics courses
in business school curricula. J. Business Ethics 10: 211-219.

Snyder, E. Y., and J. F. Luring. 2006. Beyond fraud - Stem-cell research continues. New Engl. J. Med. 354: 321-324. Wager, E., S. Fiack, C. Graf, A. Robinson, and I. Rowlands, 2Q09. Science, journal editors' views on publication ethics: results of an international survey. J. Med. Ethics 35: 348-53.
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