Exposing students to carnivorous plants within course-based undergraduate research can heighten student interest in plants and create a foundation on which to build future student projects. Carnivorous plants derive nutrients by trapping animals, but unlike most other predators, they lack mobility and are thought to attract prey through a combination of visual and olfactory cues. As part of a semester-long undergraduate research project for a junior/senior-level plant ecology class, students used carnivorous plants and artificial traps to test the importance of visual cues in the capture of wild-type and visually impaired (w1118) Drosophila melanogaster. Over the 13-week semester, students worked in groups to generate questions, design experiments, analyze data, and present results both orally and in a written manuscript. A major focus was developing students' ability to compare their results with the literature. Upon completion, manuscripts were uploaded to a digital archive for use by future students in designing projects. This database of readily accessible past projects provides students with an accessible literature base that enables them to build upon previous work in a way that more accurately reflects real-world research.

Introduction

Since 1999, the advanced Terrestrial Plant Ecology class at Augustana University has exposed students to semester-long research experiences. At first, considerable time was needed to sell the benefits of open-ended research over traditionally structured or “cookbook” laboratories (Brownell et al., 2012). Although research experiences within introductory biology courses are still considered rare (Spell et al., 2014), the increase in inquiry-based labs in introductory courses at Augustana, coupled with more independent projects in advanced courses and greater summer research opportunities, has changed the culture sufficiently so that course-based research experiences appear to be more readily accepted. Course-based undergraduate research experiences provide many of the same benefits associated with research internships, including increased analytical skills (Jordan et al., 2014) and increased communication skills (Shaffer et al., 2010; Jordan et al., 2014); however, students still struggle with many aspects of conducting research and writing a manuscript. In particular, connecting the results of their research to the literature can be challenging even for upper-level college students.

Utilizing carnivorous plants within a course-based undergraduate research experience can increase student interest and can also help address student misconceptions. Because a common perception of predator–prey relationships is that of an active animal predator, such as a lion chasing a zebra, many people may have difficulty imagining predator–prey relationships with stationary predators. Even early botanists were reluctant to accept the discovery of carnivorous plants and questioned whether photosynthetic organisms could consume insects or small animals (Juniper et al., 1989; Ellison & Gotelli, 2001). Despite being stationary, these pernicious predatory plants are effective carnivores that actively attract prey. Because carnivorous plants live in low-nutrient habitats (Juniper et al., 1989), they have evolved elaborate structures to obtain supplemental nutrients, digesting a range of arthropod orders (Juniper et al., 1989; Chin et al., 2014). Prey capture increases growth and photosynthetic efficiency, influences earlier flowering, and increases seed production (Jürgens et al., 2009; Moran & Clarke, 2010).

Our work with carnivorous plants began after a student, Cathryn Carney, was exposed to wild-type (WT) Oregon R and visually impaired “white-eyed” (w1118) fly lines in a genetics course and asked which would be more likely to be caught by carnivorous plants. It has been suspected for over a century that carnivorous species attract prey with a combination of olfactory and visual cues (Darwin, 1875; Joel et al., 1985; Juniper et al., 1989), and it is commonly accepted that the olfactory cues secreted by the plants play a vital role in attracting prey. Studies by Jürgens et al. (2009) and Di Giusto et al. (2010) found that some species of carnivorous plants are capable of mimicking compounds typically emitted by flowering plants or fruits. However, there has been disagreement over the relative importance of visual cues. For example, some studies have indicated that the red coloration of pitcher traps is important in the attraction process (Schaefer & Ruxton, 2008), while other studies have concluded that red coloration does not provide important signals for prey attraction or for camouflage of traps (Bennett & Ellison, 2009; Foote et al., 2014). Other studies have indicated that visual cues within the UV light range rather than the visible range are critical in the attraction process (Kurup et al., 2013).

Having access to literature on a topic can dramatically improve the breadth and depth of questions asked in semester-long authentic undergraduate research experiences; however, it can be challenging to find relevant literature that matches student projects. By developing a database of past projects, students have access to a literature base they can use to develop their own projects and to write their discussion.

Research Experience Setup

The Terrestrial Plant Ecology class at Augustana University includes 3 hours of lecture each week as well as 3 hours of laboratory. The laboratory is almost entirely devoted to conducting independent research projects. These semester-long research experiences culminate in journal-style manuscripts that are “published” in a class publication, “Journal of Terrestrial Plant Ecology.” In addition, students present their work in a class symposium, open to the entire campus community, at the end of the semester.

Objectives

The learning objectives of the Terrestrial Plant Ecology class include

  1. Students will demonstrate an ability to identify patterns, form and test hypotheses, design experiments, analyze data, and present conclusions (both oral and written).

  2. Students will write like a biologist, persuading readers of a researched hypothesis.

  3. Students will think critically in written form, summarizing and interpreting ecological literature.

These objectives align with several of the Science and Engineering Practices within the Next Generation Science Standards (NGSS Lead States, 2013), including planning and carrying out investigations, analyzing and interpreting data, engaging in arguments from evidence, and obtaining, evaluating, and communicating information. These objectives also align with the core competencies outlined within Vision and Change (AAAS, 2011). Specifically, they align with the abilities to apply the process of science, use quantitative reasoning, and communicate science.

Stages & Timetable of Projects

There were four distinct stages to the research experiences. These stages were similar to the four-step pedagogical framework for authentic scientific research published by McLaughlin and Coyle (2016), but differed in that the design of the experiments preceded learning experimental techniques (Table 1). While many inquiry-based experiences have focused on a particular experimental technique, the focus within the Terrestrial Plant Ecology class was on the experimental questions. Students therefore had a great deal of freedom in picking projects of interest, which increased their sense of ownership. This sense of ownership can be an important component in motivating student interest in learning (Hidi & Harackiewicz, 2000; Miller, 2008). The time required for each stage can vary depending on the project and student group, but Table 1 represents a typical sequence of events.

Table 1.
Stages and timeline for semester undergraduate research experiences.
Stages 
Stage 1: Formation of groups and crafting of project 
Stage 2: Learning techniques/data collection 
Stage 3: Data analysis 
Stage 4: Writing manuscript drafts 
Timeline Stage 1 Stage 2 Stage 3 Stage 4 
Week 1 Introduction to independent projects/brainstorm ideas for project    
Week 2 Project “speed dating” activity/formation of teams/introduction to primary literature    
Week 3 Project proposal due (includes primary literature)/meet with groups about projects   
Week 4 Meet with groups/collecting data    
Week 5 Meet with groups/collecting data   
Week 6 Collect data/work on introduction and methods  
Week 7 Collect data/first draft of introduction/methods due  
Week 8 Second draft of introduction/methods due    
Week 9 First draft of results/discussion due   
Week 10 Second draft of manuscript due/group critique of manuscripts    
Week 11 Work on presentations/work on manuscript drafts    
Week 12 Review project presentations/third draft of manuscript due    
Week 13 Project presentations/final manuscript due    
Stages 
Stage 1: Formation of groups and crafting of project 
Stage 2: Learning techniques/data collection 
Stage 3: Data analysis 
Stage 4: Writing manuscript drafts 
Timeline Stage 1 Stage 2 Stage 3 Stage 4 
Week 1 Introduction to independent projects/brainstorm ideas for project    
Week 2 Project “speed dating” activity/formation of teams/introduction to primary literature    
Week 3 Project proposal due (includes primary literature)/meet with groups about projects   
Week 4 Meet with groups/collecting data    
Week 5 Meet with groups/collecting data   
Week 6 Collect data/work on introduction and methods  
Week 7 Collect data/first draft of introduction/methods due  
Week 8 Second draft of introduction/methods due    
Week 9 First draft of results/discussion due   
Week 10 Second draft of manuscript due/group critique of manuscripts    
Week 11 Work on presentations/work on manuscript drafts    
Week 12 Review project presentations/third draft of manuscript due    
Week 13 Project presentations/final manuscript due    

During the first stage, students formed groups based on shared interests and met with the instructor weekly to craft the project (Table 1). Students were introduced to primary literature and to elements of best practices for scientific writing. They were also exposed to previous class research and encouraged to use that research as a starting place in designing their own projects. Exposure to previous class research provided groups with an accessible literature base to form hypotheses with a clear biological basis. Groups of one or two students were expected to test one primary question and a second follow-up question. For each additional student member (up to four), an additional question/hypothesis was expected to be tested. Multiple meetings between the instructor and groups ensured that the methods of planned data collection matched the questions being asked by the students. In stage 2 (Table 1), students learned and practiced the techniques needed for their projects. For some projects, the literature suggested experimental techniques, while other projects required the students and instructor to develop their own techniques. Student groups were given the freedom to decide when to schedule their data collection. Most groups scheduled data collection during the 3-hour laboratory period, whereas other groups collected data at other times during the week or during weekends. The multiple meetings during stage 1 and the beginning of stage 2 helped the instructor ensure that the data collected would be sufficient to “tell a story.” The four to five weeks allocated for data collection were typically sufficient, especially if students were able to utilize methods practiced by previous groups. During the data collection stage, preliminary data analysis was also done that might modify the follow-up/secondary questions. During stages 2 and 3, initial drafts of various sections of the manuscript were submitted.

A critical aspect of stage 4 was rewriting the manuscript drafts. The timeline includes a detailed schedule of draft due dates (Table 1). The drafts received rigorous critiquing by the instructor but were not graded, and students received completion points if they met the minimum criteria. This has similarities to an “all or nothing” grading system (Morgan et al., 2011). All drafts were handed in at the end of the semester to ensure that the students were making the requested changes. Because the instructor was an active participant in the design of projects as well as in manuscript writing, the instructor was listed as a coauthor on the paper. This changed the role of the instructor from that of a grader/evaluator to a partner/mentor in the process. This posed some risks and required a balancing act by the instructor to give enough feedback for appropriate changes, but not so much feedback that the instructor was writing the manuscript. If the instructor became the primary writer, this would likely have a negative effect on student learning (Neman, 1995) and might result in the students taking on a passive role. It was considered best practice for the instructor to maintain as much as possible that writing choices were left to the students (Brannon & Knoblauch, 1982). At the same time, mentoring by the instructor was a significant learning tool, as some students did not know how to begin and had difficulty envisioning the final product. Exposure to previous students' manuscripts also proved useful in providing a template to understand the components of a research-style manuscript and to write their discussion (Miller, 2008). For the instructor, the initial editing of manuscripts typically involved outlining the drafts, rearranging content, organizing paragraphs, and adding missing components. Critiquing of later drafts typically involved minor editorial changes, but also higher-level assistance such as explaining results within the context of the scientific literature.

Students were provided with the final manuscript rubric at the beginning of the semester and used it to critique manuscripts from other groups (Table 2). The real value of the peer review process was that it gave students experience with using the rubrics; this gave them a better understanding of how to improve their own manuscripts. The rubric was distinctive because it allocated points for writing (voice, grammar, sentence structure, etc.) within each section (introduction, methods, results, discussion) rather than for the manuscript as a whole. This was helpful because groups often divided up work by sections, and writing mechanics often varied significantly by section. In addition, the introduction and discussion typically have a different writing style than either the methods or results. A second distinctive aspect was that the rubric allocated points for primary and secondary questions, novelty of the research, and evidence of improvement. The iterative nature of science and the concept that experiments often lead to more questions was sometimes difficult for students to embrace. These points provided a positive reinforcement in getting students to see that there were always more questions to ask.

Table 2.
Final manuscript rubric for undergraduate research manuscripts.
Final Project KeyPossible Points
Title Page  
 A. Title, authors, address of institution 1.0 
Abstract  
 A. Interesting opening/clear rationale/objectives for project 1.0 
 B. Concise description of main findings 1.0 
 C. Main conclusions, and wider implications of the study 1.0 
 D. Voice is consistent – usually third person, past tense 0.5 
 E. Work is free of grammatical errors 0.5 
 F. Sentences/word choice are varied, fluent, and effective 0.5 
 G. 250 words max 0.5 
Introduction  
 A. Engaging opening 2.0 
 B. Background: ideas coherent, logical, and organized 6.0 
 C. Multiple/appropriate references in intro 5.0 
 D. Clear/appropriate objectives 3.0 
 E. Voice is consistent – usually third person, past tense 1.0 
 F. Work is free of grammatical errors 1.0 
 G. Sentences/word choice are varied, fluent, and effective 1.0 
Methods  
 A. Describe site/study organism 2.0 
 B. Describe experimental design (replication/treatments) 3.0 
 C. Describe methods (techniques/instruments, etc.) 3.0 
 D. Describe statistics 2.0 
 E. Voice is consistent – usually third person, past tense 1.0 
 F. Work is free of grammatical errors 1.0 
 G. Sentences are concise avoiding repetition of details 1.0 
 H. Writing is clearly and logically organized 1.0 
Results  
 A. Describe general patterns in tables/graphs. Highlight key points 3.0 
 B. Compare and contrast/use active language, varied, fluent 2.0 
 C. Use appropriate graphs/tables, each with labels/legends 10 
 D. Clearly explain statistical differences 2.0 
 E. Voice is consistent – usually third person, past tense 1.0 
 F. Work is free of grammatical errors 1.0 
 G. Writing is clearly and logically organized 1.0 
Discussion  
 A. Engaging opening to discussion 1.0 
 B. Clear discussion of points, ideas well supported, organized, logical 6.0 
 C. Tie back to intro. Discuss results within context of literature 5.0 
 D. Clear summary/implications 3.0 
 E. End with strong statement/argument 1.0 
 F. Voice is consistent – usually third person, past tense 1.0 
 G. Work is free of grammatical errors 1.0 
 H. Sentences/word choice are varied, fluent, and effective 1.0 
References  
 A. Complete list. Proper format, alphabetized, citations in text 5.0 
Effort/Novelty/Overall  
 A. Proper headings and page numbers 2.0 
 B. Is there a strong primary question? 4.0 
 C. Is there a secondary/follow-up question? 3.0 
 D. Does the research have novel aspects? 4.0 
 E. Is there evidence of overall effort/improvement through drafts? 4.0 
Total 100 
Final Project KeyPossible Points
Title Page  
 A. Title, authors, address of institution 1.0 
Abstract  
 A. Interesting opening/clear rationale/objectives for project 1.0 
 B. Concise description of main findings 1.0 
 C. Main conclusions, and wider implications of the study 1.0 
 D. Voice is consistent – usually third person, past tense 0.5 
 E. Work is free of grammatical errors 0.5 
 F. Sentences/word choice are varied, fluent, and effective 0.5 
 G. 250 words max 0.5 
Introduction  
 A. Engaging opening 2.0 
 B. Background: ideas coherent, logical, and organized 6.0 
 C. Multiple/appropriate references in intro 5.0 
 D. Clear/appropriate objectives 3.0 
 E. Voice is consistent – usually third person, past tense 1.0 
 F. Work is free of grammatical errors 1.0 
 G. Sentences/word choice are varied, fluent, and effective 1.0 
Methods  
 A. Describe site/study organism 2.0 
 B. Describe experimental design (replication/treatments) 3.0 
 C. Describe methods (techniques/instruments, etc.) 3.0 
 D. Describe statistics 2.0 
 E. Voice is consistent – usually third person, past tense 1.0 
 F. Work is free of grammatical errors 1.0 
 G. Sentences are concise avoiding repetition of details 1.0 
 H. Writing is clearly and logically organized 1.0 
Results  
 A. Describe general patterns in tables/graphs. Highlight key points 3.0 
 B. Compare and contrast/use active language, varied, fluent 2.0 
 C. Use appropriate graphs/tables, each with labels/legends 10 
 D. Clearly explain statistical differences 2.0 
 E. Voice is consistent – usually third person, past tense 1.0 
 F. Work is free of grammatical errors 1.0 
 G. Writing is clearly and logically organized 1.0 
Discussion  
 A. Engaging opening to discussion 1.0 
 B. Clear discussion of points, ideas well supported, organized, logical 6.0 
 C. Tie back to intro. Discuss results within context of literature 5.0 
 D. Clear summary/implications 3.0 
 E. End with strong statement/argument 1.0 
 F. Voice is consistent – usually third person, past tense 1.0 
 G. Work is free of grammatical errors 1.0 
 H. Sentences/word choice are varied, fluent, and effective 1.0 
References  
 A. Complete list. Proper format, alphabetized, citations in text 5.0 
Effort/Novelty/Overall  
 A. Proper headings and page numbers 2.0 
 B. Is there a strong primary question? 4.0 
 C. Is there a secondary/follow-up question? 3.0 
 D. Does the research have novel aspects? 4.0 
 E. Is there evidence of overall effort/improvement through drafts? 4.0 
Total 100 

Digital Archive

At the end of the semester, student groups formatted their manuscripts according to our guidelines and submitted a digital version, which was placed in Augustana University's digital archive. The archive, called Northern Plains Peoples and Places or NP3 (http://np3.augie.edu), uses the ContentDM software platform and serves as the institutional repository (IR) for scholarly content created by members of the Augustana community. The student manuscripts were arranged by year within the “Journal of Terrestrial Plant Ecology” and added to the Augustana Student Research collection in .pdf file format, which is full-text searchable. Using Dublin Core standards, key metadata elements were added, including authors, dates, tables of contents, and subject headings. The images of this collection are currently restricted to on-campus viewing, but the metadata are discoverable via Google and other web search engines.

Materials & Methods for Fruit Fly & Carnivorous Plant Projects

Drosophila melanogaster was chosen as the prey because it was readily accessible and is commonly captured by carnivorous plants in the wild (Juniper et al., 1989). Both wild-type (WT, Oregon R) and visually impaired (w1118) Drosophila melanogaster were obtained from Bloomington Stock Center (Indiana). The w1118 flies had a spontaneous loss of function allele with no functional gene product, or significantly lower product compared to WT, resulting in visual impairment (McQuilton et al., 2012). Both WT and w1118 flies were raised in standard fly media (Nutri-Fly BF), incubated at 25°C, and flipped approximately every 2 days. Second-generation flies were used whenever possible to minimize maternal effects.

Pitcher plants (Nepenthes ventricosa) and sundew plants (Drosera capensis) were obtained from California Carnivores (https://www.californiacarnivores.com) and grown in 0.5 L pots under grow lights on the Augustana University campus in Sioux Falls, South Dakota. Sundews were planted in a 3:1 peat moss and perlite mixture and pitcher plants in a 2:1:1 peat moss, perlite, and orchid bark mix. Sundews were watered twice a week from below using a tray, and pitcher plants were watered 5 days a week until water ran out the bottom of the pot.

For the projects exploring the importance of visual cues in the capture process, WT and w1118 flies were exposed to carnivorous plants, either N. ventricosa or D. capensis, or to artificial traps (Figure 1). Between 30 and 60 flies were placed in 37 L aquariums for 8 hours at ~22°C, with fluorescent overhead lighting. Total numbers of fly captures were counted, and this was repeated three to six times. Artificial traps were constructed using white, black, or red construction paper. Traps consisted of opaque 125 mL flasks and containing standard cornmeal media (Bloomington recipe) or ~1 g of overripe banana.

Figure 1.

Experimental setup. Between 30 and 60 fruit flies were released into a 37 L aquarium with either a carnivorous plant or an artificial trap.

Figure 1.

Experimental setup. Between 30 and 60 fruit flies were released into a 37 L aquarium with either a carnivorous plant or an artificial trap.

Student Survey

During the fall semester of 2017, a Google survey was created and approved by the Augustana Institutional Review Board. A link to the Google survey with questions that aligned with several of the Next Generation Science Standards was sent to a total of 71 students who had taken the Terrestrial Plant Ecology course between 2013 and 2017. Thirty-two students responded, for a 45% return rate.

Results & Discussion

Since the Terrestrial Plant Ecology course began incorporating embedded research, it has been exciting to see how students can connect and build upon previous projects. The original carnivorous plant/fruit fly project asked whether visually impaired or WT flies were caught more frequently by carnivorous plants (Carney et al., 2013). That initial project has resulted in seven different carnivorous-plant-related class projects over the past five years (Table 3), which illustrates how projects can build on previous work. In addition to studying the importance of visual cues on the capture process, student projects ranged from studying the microbiota found on carnivorous plants to looking at the effect of light intensity or wavelength on the capture process. Two students decided to continue working on their projects on their own or as part of a summer research project. They were both able to present their results at national Ecological Society of America meetings (Carney et al., 2013; Antonson et al., 2016). This illustrates how students can take ownership of the projects.

Table 3.
Student projects building off the original 2012 fruit fly carnivorous plant project. The projects were published in the class Journal of Terrestrial Plant Ecology (JTPE). PDFs are available from steven.matzner@augie.edu.
YearTitleAuthorsReference
2012 Are fruit flies attracted to carnivorous plants through visual or olfactory cues? Carney, C., Lloyd, A.J., Vander Windt, J. & Matzner, S.L. JTPE, 2, 25–38. 
2013 Fatal attraction: Are fruit flies attracted to carnivorous plants through visual or olfactory cues? Carney, C., Lloyd, A.J., Vander Windt, J. & Matzner, S.L. Abstract, Ecological Society of America Meeting 
2013 Catch me if you can: Does the level of fruit fly activity have an effect on avoiding carnivorous plants? Wodzinski, R., Teferra, H., Miles, C. & Matzner, S.L. JTPE, 3, 1–9 
2013 Setting the trap: Bacterial genera and possible symbioses in the bacterial communities and changes with pitcher age within Nepenthes ventricosa plants Schroeder, D., Egland, P. & Matzner, S.L. JTPE, 3, 10–21. 
2014 Effects of light on Drosophila melanogaster capture rate efficiency in the tropical carnivorous plants, Nepenthes ventricosa and Drosera capensis Clark, H. & Matzner, S.L. JTPE, 4, 21–29 
2015 Don't go toward the light! The visual attraction of Drosophila melanogaster to UV-fluorescence Antonson, N., Shroll, K., Snyder, C., Van Essen, M., Matzner, S.L. & Miles, C. JTPE, 5, 1–14 
2015 Microbial associations of Drosera capensis Charbonnequ, B., Surratt, C. & Matzner, S.L JTPE, 5, 48–55. 
2016 A sticky situation: The effect of light level on capture rates of Drosera capensis Foss, K., Matzner, D., Mohan, D. & Matzner, S.L. JTPE, 6, 1–13. 
2016 Learning outcomes of streaking on campus: Isolation, characterization, and analysis of N. ventricosa pitcher
microbiota 
Chandra, S., Meyer, E., Schmidtman, D. & Matzner, S.L. JTPE, 6, 14–26. 
2016 Fatal attraction: The visual attraction of Drosophila melanogaster to UV-fluorescence Antonson, N., Shroll, K., Snyder, C., Van Essen, M., Miles, C. & Matzner, S.L. Abstract, Ecological Society of America Meeting 
YearTitleAuthorsReference
2012 Are fruit flies attracted to carnivorous plants through visual or olfactory cues? Carney, C., Lloyd, A.J., Vander Windt, J. & Matzner, S.L. JTPE, 2, 25–38. 
2013 Fatal attraction: Are fruit flies attracted to carnivorous plants through visual or olfactory cues? Carney, C., Lloyd, A.J., Vander Windt, J. & Matzner, S.L. Abstract, Ecological Society of America Meeting 
2013 Catch me if you can: Does the level of fruit fly activity have an effect on avoiding carnivorous plants? Wodzinski, R., Teferra, H., Miles, C. & Matzner, S.L. JTPE, 3, 1–9 
2013 Setting the trap: Bacterial genera and possible symbioses in the bacterial communities and changes with pitcher age within Nepenthes ventricosa plants Schroeder, D., Egland, P. & Matzner, S.L. JTPE, 3, 10–21. 
2014 Effects of light on Drosophila melanogaster capture rate efficiency in the tropical carnivorous plants, Nepenthes ventricosa and Drosera capensis Clark, H. & Matzner, S.L. JTPE, 4, 21–29 
2015 Don't go toward the light! The visual attraction of Drosophila melanogaster to UV-fluorescence Antonson, N., Shroll, K., Snyder, C., Van Essen, M., Matzner, S.L. & Miles, C. JTPE, 5, 1–14 
2015 Microbial associations of Drosera capensis Charbonnequ, B., Surratt, C. & Matzner, S.L JTPE, 5, 48–55. 
2016 A sticky situation: The effect of light level on capture rates of Drosera capensis Foss, K., Matzner, D., Mohan, D. & Matzner, S.L. JTPE, 6, 1–13. 
2016 Learning outcomes of streaking on campus: Isolation, characterization, and analysis of N. ventricosa pitcher
microbiota 
Chandra, S., Meyer, E., Schmidtman, D. & Matzner, S.L. JTPE, 6, 14–26. 
2016 Fatal attraction: The visual attraction of Drosophila melanogaster to UV-fluorescence Antonson, N., Shroll, K., Snyder, C., Van Essen, M., Miles, C. & Matzner, S.L. Abstract, Ecological Society of America Meeting 

The overall goal of the student survey was to obtain evidence that students were becoming more confident in skills associated with course-based undergraduate research. The questions used were largely based on the Next Generation Science Standards. Questions were also added to the survey to assess the level of student engagement, project ownership, and whether perceptions differed depending on prior research experience. Assessment of the student experiences within the Terrestrial Plant Ecology course (n = 32 out of 71 students, 2011–2016) indicated that the majority of students either agreed or strongly agreed (higher Likert scores) that they enjoyed working on the projects, felt ownership of the projects, felt more like scientists, and that the experience increased their interest in research (Table 4). The students generally agreed that they felt more confident in their ability to form hypotheses, design and conduct experiments, utilize spreadsheets, interpret data, and write scientific-style research manuscripts (including the discussion and comparing their results with the literature). The majority also agreed or strongly agreed that the experience increased their ability to explain data, assess whether they can support their explanation of the data, and communicate scientific information in various forms (Table 4). The lowest Likert scores were in the use of statistical tools (Table 4), which will be an area of improvement for future classes. For about two-thirds of the class (62%), this independent project was their only research experience. Approximately 38% of the class had prior summer research experience. Comparisons between these two groups yielded a few significant differences, such as when analyzing the survey item “This was the most significant research experience. …” Students without a summer research experience were more likely (P < 0.007) to agree or strongly agree (Likert score averaged 4.1 on a 5.0 scale) than students who had a summer research experience (Likert score averaged 2.6). One surprise was that a significantly higher percentage of students from the non-summer research group agreed or strongly agreed with the statements “I felt more confident in my ability to use graphing tools to analyze patterns after this experience” (P < 0.0006) and “This experience increased my ability to communicate and present scientific information graphically and visually” (P < 0.0048). Overall, the survey indicated that the students had a very positive experience with the projects and felt that the projects increased their confidence in performing many of the skills associated with conducting research and writing a scientific-style research paper.

Table 4.
Student survey questions and Likert scores based on a 5.0 scale.
QuestionLikert ScoreNext Generation Science Standards
I enjoyed working on the independent project. 4.42  
I felt ownership of the project. 4.67  
This experience made me feel like a scientist. 4.42  
This was the most significant research experience (most impactful to me) that I participated in while at Augustana. 3.33  
This experience increased my interest in research. 4.09  
I felt more confident in my ability to plan and conduct a scientific investigation after this experience. 4.55 Planning & carrying out investigations 
I felt more confident in my ability to formulate hypotheses after this experience. 4.21 Planning & carrying out investigations 
I felt more confident in my ability to design treatments to test hypotheses after this experience. 4.33 Planning & carrying out investigations 
I felt more confident in my ability to use spreadsheets to organize data after this experience. 4.00 Analyzing & interpreting data 
I felt more confident in my ability to use graphing tools to analyze patterns after this experience. 3.71 Analyzing & interpreting data 
I felt more confident in my ability to use statistical tools to test hypotheses after this experience. 3.58 Analyzing & interpreting data 
I felt more confident in my ability to understand how statistics is used to analyze and interpret data after this experience. 4.06 Analyzing & interpreting data 
This experience increased my ability to explain the data collected and support that explanation with evidence. 4.36 Engaging in argument from evidence 
This experience increased my ability to assess whether data and/or literature supported my explanation of the results. 4.27 Engaging in argument from evidence 
I felt more confident in my ability to write a scientific-style research paper after this experience. 4.36 Obtaining, evaluating & communicating information 
After this experience, I felt more confident in my ability to write the discussion section of a scientific-style research paper. 4.39 Obtaining, evaluating & communicating information 
After this experience, I had a better understanding of how to compare the results of my project to what is known within the literature. 4.33 Obtaining, evaluating & communicating information 
This experience increased my ability to gather, read, and evaluate scientific information from the literature. 4.21 Obtaining, evaluating & communicating information 
This experience increased my ability to communicate scientific information in a professional oral presentation. 4.24 Obtaining, evaluating & communicating information 
This experience increased my ability to communicate and present scientific information graphically and visually. 4.12 Obtaining, evaluating & communicating information 
This experience increased my ability to communicate scientific information in written form. 4.24 Obtaining, evaluating & communicating information 
QuestionLikert ScoreNext Generation Science Standards
I enjoyed working on the independent project. 4.42  
I felt ownership of the project. 4.67  
This experience made me feel like a scientist. 4.42  
This was the most significant research experience (most impactful to me) that I participated in while at Augustana. 3.33  
This experience increased my interest in research. 4.09  
I felt more confident in my ability to plan and conduct a scientific investigation after this experience. 4.55 Planning & carrying out investigations 
I felt more confident in my ability to formulate hypotheses after this experience. 4.21 Planning & carrying out investigations 
I felt more confident in my ability to design treatments to test hypotheses after this experience. 4.33 Planning & carrying out investigations 
I felt more confident in my ability to use spreadsheets to organize data after this experience. 4.00 Analyzing & interpreting data 
I felt more confident in my ability to use graphing tools to analyze patterns after this experience. 3.71 Analyzing & interpreting data 
I felt more confident in my ability to use statistical tools to test hypotheses after this experience. 3.58 Analyzing & interpreting data 
I felt more confident in my ability to understand how statistics is used to analyze and interpret data after this experience. 4.06 Analyzing & interpreting data 
This experience increased my ability to explain the data collected and support that explanation with evidence. 4.36 Engaging in argument from evidence 
This experience increased my ability to assess whether data and/or literature supported my explanation of the results. 4.27 Engaging in argument from evidence 
I felt more confident in my ability to write a scientific-style research paper after this experience. 4.36 Obtaining, evaluating & communicating information 
After this experience, I felt more confident in my ability to write the discussion section of a scientific-style research paper. 4.39 Obtaining, evaluating & communicating information 
After this experience, I had a better understanding of how to compare the results of my project to what is known within the literature. 4.33 Obtaining, evaluating & communicating information 
This experience increased my ability to gather, read, and evaluate scientific information from the literature. 4.21 Obtaining, evaluating & communicating information 
This experience increased my ability to communicate scientific information in a professional oral presentation. 4.24 Obtaining, evaluating & communicating information 
This experience increased my ability to communicate and present scientific information graphically and visually. 4.12 Obtaining, evaluating & communicating information 
This experience increased my ability to communicate scientific information in written form. 4.24 Obtaining, evaluating & communicating information 

Conclusions

This example of course-based research illustrates how student projects can build upon each other and how the questions arising from one research project can provide the basis for future student projects. Providing students access to a database of previous student projects gives them a powerful tool that helps them design their own projects and creates a more authentic research experience. Through these carnivorous plant projects, student groups discovered that visual cues (particularly within the UV spectrum) can have a significant effect in attracting prey to a particular trap. Results of the student survey confirmed that students felt ownership of their projects and that they felt more confident in skills related to planning and carrying out investigations; analyzing and interpreting data; and obtaining, evaluating, and communicating information. The survey also identified some areas of improvement in the implementation of the projects, such as providing more training with statistical tools, and indicated some differences between students with prior research experience and those without. The use of course-based research, coupled with a focus on writing the discussion, can enhance the ability of students to apply the process of science, use quantitative reasoning, and communicate science. These are important goals that have been expressed both in the Next Generation Science Standards and within the Vision and Change report.

This research was supported in part by an Institutional Development Award (IDeA) from the National Institute of General Medical Sciences of the National Institutes of Health (P20GM103443) as well as funding from the National Science Foundation/EPSCoR program (IIA-1355423) and the State of South Dakota. The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health or the National Science Foundation. We are also thankful for all the support from Augustana faculty who helped in the mentoring of students for their independent projects and all the students who worked so hard on these projects. Thanks also to many people who gave feedback on various stages of the manuscript, including Emma Miller, Grady Carlisle, Dr. Anna George, and Dr. Anne-Marie Hoskinson.

References

References
AAAS
(
2010
).
Vision and Change in Undergraduate Biology Education: A Call to Action
.
Washington, DC
:
American Association for the Advancement of Science
. http://visionandchange.org/files/2011/03/Revised-Vision-and-Change-Final-Report.pdf.
Antonson, N., Shroll, K., Snyder, C., Van Essen, M., Miles, C. & Matzner, S.L. (
2016
).
Fatal attraction: visual attraction of Drosophila melanogaster to UV-fluorescence
. Abstract, Ecological Society of America Meeting, August 12, 2016, Ft.
Lauderdale, FL
.
Bennett, K. & Ellison, A. (
2009
).
Nectar, not colour, may lure insects to their death
.
Biology Letters
,
5
,
469
472
.
Brannon, L. & Knoblauch, C.H. (
1982
).
On students' rights to their own texts: a model of teacher response
.
College Composition and Communication
,
33
,
157
166
.
Brownell, S.E., Kloser, M.J., Fukami, T. & Shavelson, R. (
2012
).
Undergraduate biology lab courses: comparing the impact of traditionally based “cookbook” and authentic research-based courses on student lab experiences
.
Journal of College Science Teaching
,
41
,
36
45
.
Carney, C.L., Lloyd, A.J., Vander Windt, J., Matzner, S.L. & Howard, D.R. (
2013
).
Fatal attractions: the influence of prey sensory modality on capture rates in insectivorous plants
. Abstract, Ecological Society of America Meeting, August 8, 2013,
Minneapolis, MN
.
Chin, L., Chung, A.Y. & Clarke, C. (
2014
).
Interspecific variation in prey capture behavior by co-occurring Nepenthes pitcher plants: evidence for resource partitioning or sampling-scheme artifacts?
Plant Signaling & Behavior
,
9
,
e27930
.
Darwin, C. (
1875
).
Insectivorous Plants
.
London
:
John Murray
.
Di Giusto, B., Bessière, J.M., Guéroult, M., Lim, L.B.L., Marshall, D.J., Hossaert-McKey, M. & Gaume, L. (
2010
).
Flower-scent mimicry masks a deadly trap in the carnivorous plant Nepenthes rafflesiana
.
Journal of Ecology
,
98
,
845
856
.
Ellison, A.M. & Gotelli, N.J. (
2001
).
Evolutionary ecology of carnivorous plants
.
Trends in Ecology & Evolution
,
16
,
623
629
.
Foote, G., Rice, S.P. & Millet, J. (
2014
).
Red trap colour of the carnivorous plant Drosera rotundifolia does not serve a prey attraction or camouflage function
.
Biological Letters
,
10
, 20131024.
Hidi, S. & Harackiewicz, J.M. (
2000
).
Motivating the academically unmotivated: A critical issue for the 21st century
.
Review of Educational Research
,
70
,
151
179
.
Joel, D.M., Juniper, B. & Dafni, A. (
1985
).
Ultraviolet patterns in the traps of carnivorous plants
.
New Phytologist
,
101
,
585
593
.
Jordan, T.C., Burnett, S.H., Carson, S., Caruso, S.M., Clase, K., DeJong, R.J., et al (
2014
).
A broadly implementable research course in phage discovery and genomics for first-year undergraduate students
.
mBio
,
5
,
e01051
13
.
Juniper, B., Robins, R. & Joel, D. (
1989
).
The Carnivorous Plants
.
San Diego, CA
:
Academic Press
.
Jürgens, A., El-Sayed, A.M. & Suckling, D.M. (
2009
).
Do carnivorous plants use volatiles for attracting prey insects?
Functional Ecology
,
23
,
875
887
.
Kurup, R., Johnson, A.J., Sankar, S., Hussain, A.A., Sathish Kumar, C. & Sabulal, B. (
2013
).
Fluorescent prey traps in carnivorous plants
.
Plant Biology
,
15
,
611
615
.
McLaughlin, J.S. & Coyle, M.S. (
2016
).
Increasing authenticity and inquiry in the cell and molecular biology laboratory
.
American Biology Teacher
,
78
,
492
500
.
McQuilton, P., St. Pierre, S.E., Thurmond, J. &
FlyBase Consortium
(
2012
).
FlyBase 101 – the basics of navigating FlyBase
.
Nucleic Acids Research
,
40
(Database issue),
D706
D714
.
Miller, H. (
2008
).
Designing effective writing assignments
. http://writing.umn.edu/tww/assignments/designing.html.
Moran, J.K. & Clarke, C.M. (
2010
).
The carnivorous syndrome in Nepenthes pitcher plants: current state of knowledge and potential future directions
.
Plant Signaling & Behavior
,
5
,
644
648
.
Morgan, W., Fraga, D. & Macauley, W.J., Jr. (
2011
).
An integrated approach to improve the scientific writing of introductory biology students
.
American Biology Teacher
,
73
,
149
153
.
Neman, B.S. (
1995
).
Teaching Students to Write
.
Oxford, UK
:
Oxford University Press
.
NGSS Lead States
(
2013
).
Next Generation Science Standards: For States, By States
.
Washington, DC
:
National Academies Press
.
Schaefer, H.M. & Ruxton, G.D. (
2008
).
Fatal attraction: carnivorous plants roll out the red carpet to lure insects
.
Biological Letters
,
4
,
153
155
Shaffer, C.D., Alvarez, C.J., Bailey, C.P., Barnard, D., Bhalla, S.C., Chandrasekaran, C., et al (
2010
).
The Genomics Education Partnership: successful integration of research into laboratory classes at a diverse group of undergraduate institutions
.
CBE Life Sciences Education
,
9
,
55
69
.
Spell, R.M., Guinan, J.A., Miller, K.R. & Beck, C.W. (
2014
).
Redefining authentic research experiences in introductory biology laboratories and barriers to their implementation
.
CBE Life Sciences Education
,
13
,
102
110
.