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Exotic species are perceived more than native ones in a megadiverse country as brazil

Abstract

Research on environmental perception is essential for the understanding of individuals’ relations and expectations towards natural environments. Here, we evaluated the perception of high school students on exotic and native species in Brazil. We interviewed 371 students from two high schools located in the state of Goiás, one with and one without a protected area within its premises. Students needed to identify native and exotic species and to indicate species origin. We used a t-test to evaluate differences between students’ scores regarding the correctness of species origin and also ANOVA to assess whether these scores varied among taxonomic groups. Students identified exotic species better than native ones. Students better identified exotic mammals, fishes, and birds than native ones. We found there were no significant relationships of students’ knowledge of species’ origins with socioecological factors. Students’ perceptions of exotic and native species were low and focused on charismatic large-bodied species. We suggest that students are encouraged to expand their knowledge of local biodiversity. Teachers, local schools, and policymakers are essential to achieve this aim. A more diverse methodology for teaching, including new technologies and citizen-science projects, can help establish a genuine interest of local biodiversity students.

Key words
conservation; environmental education; charismatic species; protected areas; biological invasions

INTRODUCTION

Exotic species are recognized as one of the main drivers of environmental changes and biodiversity losses (Bellard et al. 2016BELLARD C, CASSEY P, BLACKBURN TM & BLACKBURN TM. 2016. Alien species as a driver of recent extinctions. Biol Lett 12: 20150623., Carruthers 2004CARRUTHERS RI. 2004. Biological control of invasive species, a personal perspective. Conserv Biol 18: 54-57., Walker & Steffen 1997WALKER BH & STEFFEN W. 1997. An overview of the implications of global change for natural and managed terrestrial ecosystems. Conserv Ecol 1: n. 2.). These species may cause considerable ecological problems as they establish, dominate, and effectively alter the natural ecosystem’s functioning (Blackburn et al. 2011BLACKBURN TM, PYŠEK P, BACHER S, CARLTON JT, DUNCAN RP, JAROŠÍK V, WILSON JRUU & RICHARDSON DM. 2011. A proposed unified framework for biological invasions. Trends Ecol Evol 26: 333-339.). Moreover, exotic species cause changes in ecological interactions, local productivity rates, nutrient cycling, and community and habitat structuring, thereby leading to a reduction in native species’ populations, which in turn can drive regional and global species extinction (Pejchar & Mooney2009, Simberloff 2005SIMBERLOFF D. 2005. Non-native species do threaten the natural environment! J Agric Environ Ethics 18: 595-607.). The severe consequences that the biological invasions cause to biodiversity, human health, and well-being, along with their undeniable economic impacts (Pimentel et al. 2001PIMENTEL D ET AL. 2001. Economic and environmental threats of alien plant, animal, and microbe invasions. Agric Ecosyst Environ 84: 1-20., 2005) are increasing public awareness of the effects of exotic species (Pejchar & Mooney 2009PEJCHAR L & MOONEY HA. 2009. Invasive species, ecosystem services and human well-being. Trends Ecol Evol 24: 497-504.).

After introducing exotic invasive species, both management and control actions can be considered expensive (Mack et al. 2000MACK RN, SIMBERLOFF D, LONSDALE WM, EVANS H, CLOUT M & BAZZAZ F. 2000. Biotic invasions: Causes, epidemiology, global consequences, and control. Ecol Appl 10: 689-710., Pimentel et al. 2005PIMENTEL D, ZUNIGA R & MORRISON D. 2005 Update on the environmental and economic costs associated with alien-invasive species in the United States. Ecol Econ 52: 273-288.). The prevention of new invasions by making people aware of the harmful effects is one of the least costly ways to mitigate their effects (Wittenberg & Cock 2001WITTENBERG R & COCK MJW. 2001. Invasive alien species: A toolkit of best prevention and management practices. 17th ed., CAB International, Wallingford, Oxon, UK.). Therefore, implementing educational actions against biological invasions may avoid impacts upon natural and managed ecosystems as well as impairments to human health (Pimentel et al. 2005PIMENTEL D, ZUNIGA R & MORRISON D. 2005 Update on the environmental and economic costs associated with alien-invasive species in the United States. Ecol Econ 52: 273-288.). Such activities also allow citizens to reflect on the use of exotic species (Ziller & Zalba 2007ZILLER SR & ZALBA S. 2007. Propostas de ação para prevenção e controle. Nat Conserv 5: 8-15.), which can help raise public awareness regarding the importance of native fauna and flora (Proença et al. 2014PROENÇA MS, OSLAJ EU & DAL-FARRA RA. 2014. As percepções de estudantes do ensino fundamental em relação às espécies exóticas e o efeito antrópico sobre o ambiente. Pesqui Educ Ambient 9: 51-66.).

Scientific/environmental education represents an interactive link between science and people, arousing concern, enabling awareness, and directing viable and more effective conservation strategies concerning invasive species (Benites & Mamede 2008BENITES M & MAMEDE SB. 2008. Mamíferos e aves como instrumentos de educação e conservação ambiental em corredores de biodiversidade do Cerrado, Brasil. Mastozoología Neotrop 15: 261-271.). Environmental education (EE hereafter) must allow space for society to rethink and debate environmental problems, increase awareness and value more environmentally responsible practices, and construct more sustainable human societies (Jacobi 2003JACOBI PR. 2003. Educação ambiental, cidadania e sustentabilidade. Cad Pesqui 118: 189-205.).

Environmental perception surveys help clarify how people perceive and relate to the environment and their expectations and behaviors (Rebouças et al. 2015REBOUÇAS MA, GRILO JA & ARAÚJO CL. 2015. Percepção ambiental da comunidade visitante do Parque municipal Dom Nivaldo Monte Natal/RN. Holos 3: 109-120.). Such surveys can reveal relationships between man and nature and help effectively elaborate, plan, and implement EE activities within conservation unit facilities (CUFs hereafter), potentially causing better conservation results (Hernes & Metzger 2016HERNES MI & METZGER M. 2016. Understanding local community’s values, worldviews and perceptions in the Galloway and Southern Ayrshire Biosphere. J Environ Manage 186: 12-23., Torres & Oliveira 2008TORRES DF & OLIVEIRA ES. 2008. Percepção ambiental: Instrumento para educação ambiental em unidades de conservação. Rev Eletrônica Mestr Educ Ambient 21: 227-235.). Therefore, allied with EE, environmental perception research contributes to the determination of populational needs and proposes methodological improvements to stimulate people’s awareness of ecological problems (Palma 2005PALMA IR. 2005. Análise da percepção ambiental como instrumento ao planejamento da educação ambiental. Porto Alegre, Universidade Federal do Rio Grande do Sul, p. 24.).

Thus, previous environmental perception surveys demonstrate low public awareness regarding native biodiversity, especially when comparing the knowledge involving exotic invasive species (Amaral et al. 2017AMARAL DF, FARIA DBG, GOMES MR, SILVA AR & MALAFAIA G. 2017. Percepção sobre o bioma Cerrado (Goiás, Brasil) de estudantes do ensino médio de escolas da educação básica. Rev Port Estud Reg 45: 71-82., Bizerril & Andrade 1999BIZERRIL M X A, ANDRADE T C S. 1999. Knowledge of the urban populations about fauna: Comparison between Brazilian and exotic animals. Cienc Cult 51: 38-41., Genovart et al. 2013GENOVART M, TAVECCHIA G, ENSEÑAT JJ & LAIOLO P. 2013. Holding up a mirror to the society: Children recognize exotic species much more than local ones. Biol Conserv 159: 484-489., Lindemann-Matthies & Bose 2008LINDEMANN-MATTHIES P & BOSE E. 2008. How many species are there? Public understanding and awareness of biodiversity in Switzerland. Hum Ecol 36: 731-742.). Students show recurrent biases towards protecting exotic and/or iconic/charismatic species, whilst native ones are neglected (Ballouard et al. 2011BALLOUARD JM, BRISCHOUX F & BONNET X. 2011. Children prioritize virtual exotic biodiversity over local biodiversity. PLoS One 6: e23152., Bizerril 2004BIZERRIL MXA. 2004. Children’s perceptions of Brazilian Cerrado landscapes and biodiversity. J Environ Educ 35: 47-58., Diniz & Tomazello 2005DINIZ EM & TOMAZELLO MGC. 2005. Crenças e concepções de alunos do ensino médio sobre biodiversidade: Um estudo de caso. Assoc Bras Pesqui Educ Ciências 5: 1-12., Genovart et al. 2013GENOVART M, TAVECCHIA G, ENSEÑAT JJ & LAIOLO P. 2013. Holding up a mirror to the society: Children recognize exotic species much more than local ones. Biol Conserv 159: 484-489., Snaddon et al. 2008SNADDON JL, TURNER EC & FOSTER WA. 2008. Children’s perceptions of rainforest biodiversity: Which animals have the lion’s share of environmental awareness? PLoS One 3: e2579.). Such a trend is perceived in schools where students show a low capacity to identify native species and a high preference for domesticated/exotic species (Bizerril 2004BIZERRIL MXA. 2004. Children’s perceptions of Brazilian Cerrado landscapes and biodiversity. J Environ Educ 35: 47-58.). Ergo, applying more efforts to raise awareness and arouse the public interest regarding the importance of biodiversity and environmental problems are imperative (Lindemann-Matthies & Bose 2008LINDEMANN-MATTHIES P & BOSE E. 2008. How many species are there? Public understanding and awareness of biodiversity in Switzerland. Hum Ecol 36: 731-742.).

Therefore, we aimed to measure the perception of exotic and Brazilian native fauna by final year high school students and to evaluate the determinants of their biological perceptions. We assessed the knowledge level of the students with regards to both exotic and native fauna and related them to the following variables: the presence or absence of CUFs in the municipality’s surroundings, the knowledge on species origins of rural vs. urban students; frequency of contact with nature; participation in field classes; and preference to protect any taxonomic group.

MATERIALS AND METHODS

Data sampling

We built two questionnaires for data collection. The first one was descriptive (Supplementary Material - Descriptive Questionnaire S1) with eight subjective questions. In our second questionnaire (Quantitative Questionnaires S1 to S4 Figure S1. Answers given by students from municipality with a CU facility and municipality without a CU facility to the questions a) 6 and b) 7 of the subjective/descriptive questionnaire. Question 6 referred to the frequency of the students’ contact with nature, and question 7 referred to locations where the students have field classes in both municipalities. Table SI. The species utilized in our questionnaires considering their scientific names, popular names, taxonomic group, and status (native or exotic) in Brazil. Quantitative Questionnaire S1-S4. ), a cardboard game with images of exotic and Brazilian native animals, the students could identify the species presented to them. We chose images of 40 fauna species, downloaded from Google’s search engine (http://www.google.com.br), homogeneously covering mammals, fishes, birds, amphibians/reptiles, and invertebrates (Quantitative Questionnaires S1 to S4). We asked for specialists’ opinions from each zoological group to evaluate and indicate the species more likely to be recognized by the students before including the images in the questionnaire. We limited our dataset to native species that occur in the Brazilian Cerrado savanna, the biome in which the two cities where we conducted our survey can be found. We assumed that by constraining our species pool to those we used, we would be verifying the student’s recognition of the native species from the local fauna. We considered as exotic those species with distributions that were not found in any of the Brazilian biomes. We built four different questionnaire cards, which we distributed randomly in the classrooms. Each questionnaire card had 11 images: two from each group indicated above, one native and one exotic, and a domesticated animal (a dog or a cat). We included the domestic animal to detect potentially careless and purposely wrong answers from the students, allowing for removing his/her answers from our sampling pool. Of the four alternative answers each image had, one was correct, and the other three were incorrect. We also asked the students whether that species was native or not. Our specific questions were: 1) Are exotic species more accurately recognized than native Brazilian species? 2) Do students differentiate the species’ place of origin? 3) Do students who live in a municipality close to a CUF know more about native species than about exotic ones? 4) Do students living in rural areas know more about native species than students living in urban areas? 5) Do students who visit the CUFs know more about native species than students who do not visit them? 6) Do students know and intend to protect charismatic zoological groups (e.g., mammals) and exotic fauna more often than other taxonomic groups and native fauna? 7) Do students who have more contact with native species know more about native species? 8) Do students who participate in practical field classes (park visits, ecological trails, farm visits, etc.) know more about native species than students without such field classes?

We performed a pilot research study with six high school classes totaling 32 students in September 2017 to evaluate our questionnaires. Based on this pilot project, we first applied the subjective questionnaire and, then, the questionnaire cards to avoid interference of the content and images from the second questionnaire upon students’ answers in the subjective questionnaire.

We sampled our data in two municipalities in the state of Goiás, Brazil: with a CUF, Silvânia (National Forest of Silvânia - FLONA), and without a CUF, Bela Vista de Goiás. Both of them were located in the same state region and share similar socioeconomic conditions. We investigated the capacity to identify exotic and Brazilian native species of 371 students of the last year of high school, being 182 students in the municipality with a CUF and 189 students in the municipality without a CUF. In the city with a CUF, we conducted surveys in three schools (one public, one private, and one public/private), while in the city without a CUF (one public and one private), we conducted two other samples. On average, each class evaluated in both of the cities had 21 students. We invited all students in the classes to our research, but only those whose parents or legal guardians authorized their participation after signing a consent form took part. Students answered the questionnaires without any prior intervention or clarification by those who applied the test regarding definitions and concepts of an exotic or a Brazilian native species. We submitted the questionnaires to the research ethics committee of Universidade Estadual de Goiás related to the Brazilian Health Ministry, which approved our procedures (process number at CAAE: 77679717.2.0000.8113). All the sampled data is available at https://github.com/hersonpc/mestrado-exoticas-nativas.

Data treatment and analyses

We evaluated and classified each question from our descriptive questionnaire into five categories: Great (complete answer, with a clear and precise concept); Good (answer with a satisfactory concept); Regular (incomplete answer); Bad (incorrect answer); and Blank (the student left the question without any answer). We quantified the students’ answers from the cardboard image questionnaire and assigned them a numeric value. Then, we defined and calculated three metrics: A) the proportion of correct species identifications – the average proportion of correct species’ name identification; B) proportion of origin identifications – the average proportion of correct identification of each species’ origin; C) recognition rate – the correct association between the proportion of species’ names identification and origin identifications, which we only calculated when the evaluated student correctly marked both species’ name and origin answers. We calculated the recognition rate to verify the accuracy of students’ scores between both previous metrics and compared each of the interviewees’ responses in relation to the correct answers between exotic and native species.

We processed and analyzed our data in R 3.4.3 (R Development Core Team 2018R DEVELOPMENT CORE TEAM. 2018. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Viena, Austria.) using the packages dplyr, stringr, reshape2, ggplot2, gridExtra, knitr, kableExtra, nortest, and stats. We used dependent t-tests to evaluate whether the 1) Students reached higher scores while identifying the name of exotic species than Brazilian native species; 2) Students reached higher scores while identifying the origins of exotic species than that of Brazilian native species; 3) Students living in the city close to a CUF attained higher scores while identifying Brazilian native species than when identifying exotic species compared to students living in a city without a CUF; 4) Students residing in rural areas reach higher scores while identifying Brazilian native species than exotic species compared to students residing in urban areas; 5) Students visiting the CUFs attained higher identification scores of Brazilian native species than students that do not visit the CUFs. We used a hierarchical ANOVA to test if 6) Students have higher scores and intend to protect large-bodied and exotic fauna components than smaller or less emblematic Brazilian native species; 7) Students that have a higher frequency of contact with nature would attain higher scores related to native species than to exotic ones; and 8) Students who participate in practical field classes would reach higher scores related to native species than those students without such classes. We used a post-hoc Tukey test with α=0.05 to determine the differences among the tested groups.

RESULTS

Descriptive results of our sampling pool

Female students constituted 54% of the interviewees and the students’ ages ranged from 15 to 20 years, with most of them being 17 (n=148; 40% of the total), 16 (n=133; 36%), more than 18 years (n=46; 12%) and, 15 years (n=19; 5%). Some did not disclose their ages (n=21; 6%). Among the students, 80.6% (n=299) lived in urban areas (19.4%; n=72 lived in rural areas) and had an average of 13 years of residency in each of the studied municipalities [most of the students (n=228; 62%) lived more than ten years in their municipalities.

Results from the descriptive/subjective questionnaire

Considering the question “What is an exotic species for you?”, 64% of the students’ answers were considered as wrong. The most cited concepts in this question were “it is a species that is difficult to find” and “a species that is becoming extinct”, “a rare species”, “a strange/different species”, “a lesser-known/seen species”, or “a species that lives in the woods” (Table I). In the second question, 37.6% of all students did not cite any correct example of an exotic species. In total, the students ranked 188 exotic species, with at least three Brazilian native species (the hyacinth macaw, the jaguar, and the giant anteater) being cited as exotic in the top-ten species rank. The top-twenty species cited as exotic (with some native species cited as being exotic, as well) are listed in Figure 1a.

Figure 1
Ranking of species cited by the students as examples of a) exotic species, b) Brazilian native species, and c) species that should be primarily conserved.
Table I
Classification of the students’ answers regarding the concept described in questions 1, 3, and 4 of the subjective questionnaire. The results from the other questions were discussed in the text.

For the question “Do you think exotic species cause any benefit/harm to the environment?”, 68.3% of the answers were classified as “bad”. Some of these answers were: “they neither cause benefits nor problems“, “all species are beneficial to the environments“, “species regulate the food chain“, “species maintain the biome in equilibrium“, “any species can cause harm to the environment”, or only “yes/no” answers. In the fourth question, “For you, what is a native species?”, we classified the answers as either “good” (47.6%; n=174) or “great” (31.5%; n=115; Table I).

Regarding the cited examples of Brazilian native species by the students, only 18.5% (n=67) of them incorrectly cited examples as being domestic species. In total, 152 species were cited as Brazilian natives (Figure 1b), with the most commonly cited ones being the giant anteater, the maned wolf, the hyacinth macaw, the jaguar, the pequi fruit (Caryocar brasiliensis Camb. Caryocaraceae), the armadillo, the capybara, the golden lion tamarin, “dog” (a domesticated exotic species in Brazil), and snake.

Considering the question “Cite three animal species in need for priority protection”, a total of 118 species were ranked and the top-ten species were the hyacinth macaw, the jaguar, the giant anteater, the maned wolf, the golden lion tamarin, “monkeys”, the giant panda bear, the Amazon River dolphin, the armadillo, and “dog” (Figure 1c). Among the top-10 species cited to be primarily conserved, there were 9 mammals and only one bird.

We classified the frequency of the students’ contact with nature into five categories: “never had contact“, “rarely had contact (just a few times)”, “sometimes had contact (sometimes per year)”, “often had contact (monthly contact)”, “always had contact (daily contact)”. Most of the students answered that they were “often in contact with nature” (38.7%; n=144), followed by “sometimes had contact with nature” (32.3%; n=120), “always had contact with nature” (19.9%; n=74), “rarely had contact with nature” (8.9%; n=33), and “never had contact with nature” (0.2%; n=1). Nonetheless, the municipality with a CUF stands out with a higher number of interviewees that are “often in contact with nature”, while the municipality without a CUF had a higher proportion of students claiming they are “rarely in touch with nature” (Figure S1a Figure S1. Answers given by students from municipality with a CU facility and municipality without a CU facility to the questions a) 6 and b) 7 of the subjective/descriptive questionnaire. Question 6 referred to the frequency of the students’ contact with nature, and question 7 referred to locations where the students have field classes in both municipalities. Table SI. The species utilized in our questionnaires considering their scientific names, popular names, taxonomic group, and status (native or exotic) in Brazil. Quantitative Questionnaire S1-S4. ). Sixty-one percent (n=228) of the students answered that they participated in field classes (in parks, field trails, farms, or CUF). In the municipality without a CUF, most students did not attend any field classes (47%; n=91 students), while this proportion was much smaller in the municipality with a CUF (29%; n= 52), with many students from this municipality reporting that they attended field classes at the CUFs or other ecological trails (54%; =97).

On the other hand, students from the municipality without a CUF reported that the main kind of field classes were performed at an Ecological Museum in the state capital, in Goiânia (Cerrado Memorial Museum; Figure S1b Figure S1. Answers given by students from municipality with a CU facility and municipality without a CU facility to the questions a) 6 and b) 7 of the subjective/descriptive questionnaire. Question 6 referred to the frequency of the students’ contact with nature, and question 7 referred to locations where the students have field classes in both municipalities. Table SI. The species utilized in our questionnaires considering their scientific names, popular names, taxonomic group, and status (native or exotic) in Brazil. Quantitative Questionnaire S1-S4. ). Finally, 71% of the students (n=130) from the municipality with a CUF, answered positively when asked “have you already visited the CUF?”. Among the 130 students that visited the CUFs, 40.7% had visited it only once (n=53), 24.6% visited it twice (n=32), 16% visited it three times (n=21), 5% visited it four times (n=7) and 13.7% visited it five or more times (n=17).

Results from the objective questionnaire

Students better identified exotic species when compared to native ones (t=27.00; d.f.= 370; p<0.050; Figure 2a). Nonetheless, considering the exotic and native species’ origins, the students better identified the native species’ origin in a higher proportion than the origins of exotic species (t= -16.00; d.f.= 370; p<0.050; Figure 2b). Students correctly associated the species’ identification and origin of exotic species in higher proportions than those for native species (t=7.60; d.f.= 370; p<0.050; Figure 2c).

Figure 2
Percentual average of recognition level of a) species’ name identification, b) species’ origin identification, c) recognition rate. The central point corresponds to the means, the boxes correspond to the standard error and the bars correspond to the confidence intervals at 95%.

We did not observe any effect of the students’ municipality (t=0.650, d.f.= 360, p=0.50), place of residence (rural vs. urban areas; t= -2.00, d.f.= 110, p=0.05), or having visited the CUFs or not (t=-1,60; d.f. 86; p=0.10) in the students’ perception scores of exotic and Brazilian native species.

Students reached higher scores when identifying the origins of the exotic species than when identifying native ones for all five zoological groups (F=21.7; d.f.=4; p<0.05). We observed the highest proportion of correct answers for mammals and exotic fishes, while the native fishes and invertebrates reached the lowest proportion of correct answers (Figure 3). We did not observe any effect of the frequency of contact with nature (F=0.460; d.f.=4; p=0.760) and participation in field classes (F=0.730; d.f.=6; p=0.630) upon the students’ perception of the species’ origin. The exotic species that gained the highest scores were the platypus (Ornithorhynchus anatinus), the clown-fish (Amphiprion ocellaris), and the boar (Sus scrofa), all with more than 90% of correct answers (n=96, n=96 e n=87, respectively). The native species with the highest scores by the students were the giant anteater (Myrmecophaga tridactyla), the burrowing owl (Athene cuniculaaria), and the red-legged seriema (Cariama cristata), all with more than 85% of answers being correct (n=97, n=87 and n=84, respectively).

Figure 3
Mean correct identification rate by the students, between exotic and native Brazilian species, among the five zoological groups we considered in the study. The central point corresponds to the means, the boxes correspond to the standard error and the bars correspond to the 95% confidence intervals. Different letters indicate statistical differences among the means, at a 5% probability.

DISCUSSION

Students better identified exotic species than Brazilian native ones, indicating that their perceptions of the exotic species are more robust than those for the species from their own country. Nonetheless, we observed that a significant share of students could not conceptualize and exemplify what exactly an exotic species is, given the incomplete and mistaken concepts and knowledge of benefits and problems caused by them. We highlight that the two species most cited by students as examples of exotic species were the Brazilian native hyacinth macaw and the jaguar. Students identified the origin of the native species with greater success than the exotic ones, although they did not differentiate exotic species from native ones. Thus, although they could visually identify exotic species, they have little knowledge about the concept of what defines an exotic species. We also observed no effect of municipality, place of residence, frequency of contact with nature, participating in field classes, and visiting a CUF upon the students’ perception of species. However, students better identified exotic species than their native counterparts, with exotic mammals and fishes reaching the highest scores and native fishes and invertebrates attaining the lowest ones.

A strong media appeal in television, cartoons, and movies may have influenced the higher rates of correct answers regarding exotic species (Bizerril 2004BIZERRIL MXA. 2004. Children’s perceptions of Brazilian Cerrado landscapes and biodiversity. J Environ Educ 35: 47-58., Diniz & Tomazello 2005DINIZ EM & TOMAZELLO MGC. 2005. Crenças e concepções de alunos do ensino médio sobre biodiversidade: Um estudo de caso. Assoc Bras Pesqui Educ Ciências 5: 1-12.). Such higher appeal may also be observed in textbooks that teach basic zoology to students using examples of exotic animals rather than native ones. Consequently, for many students, their first contact with the specimens from these zoological groups occur with exotic species like giraffes, elephants, and lions, species that would be exotic in Brazil, rather than studying and getting to understand some of the country’s native species (Bezerra & Suess 2013BEZERRA RG & SUESS RC. 2013. Abordagem do bioma cerrado em livros didáticos de biologia do ensino médio. Holos 1: 233-242., Silva et al. 2008SILVA FB, ROMANI R & BARANAUSKAS MCC. 2008. SOO Brasileiro: Aprendizagem e diversão no XO. Rev Bras Informática Educ 16: 29-41.). Another factor that may explain the higher recognition of exotic species is the naturalization process of these species when species were introduced a long time ago and are so present in everyday life that people begin to view them as native species (Lima et al. 2010LIMA FP, LATINI AO & DE MARCO P JR. 2010 How are the lakes? Environmental perception by fishermen and alien fish dispersal in Brazilian tropical lakes. Interciencia 35: 84-91., Vitule 2009VITULE JRS. 2009. Introdução de peixes em ecossistemas continentais brasileiros: revisão, comentários e sugestões de ações contra o inimigo quase invisível. Neotrop Biol Conserv 4: 111-122.). Therefore, naturalized species are easily recognized by the population even though they are not native to that region.

Students also incorrectly exemplified several native species as exotic, not distinguishing them from rare and/or emblematic ones. This result demonstrates that there is a lack of information regarding what an exotic species is. Therefore, both schools and different media types better must inform students and the public in general about the potential impacts and problems related to biological invasions. School teaching programs and curriculums do not usually cover such topics concerning biological invasions in Brazil’s elementary schools (Lima et al. 2010LIMA FP, LATINI AO & DE MARCO P JR. 2010 How are the lakes? Environmental perception by fishermen and alien fish dispersal in Brazilian tropical lakes. Interciencia 35: 84-91.). Lack of knowledge about exotic species raises concerning results given the relevance of this topic and the diversity of pervasive ecological (Pejchar & Mooney 2009PEJCHAR L & MOONEY HA. 2009. Invasive species, ecosystem services and human well-being. Trends Ecol Evol 24: 497-504.) and economic effects (Pimentel et al. 2001PIMENTEL D ET AL. 2001. Economic and environmental threats of alien plant, animal, and microbe invasions. Agric Ecosyst Environ 84: 1-20., 2005) caused by exotic species. Therefore, it is crucial to inform the public and government institutions that the prevention of exotic species is simpler and cheaper than controlling and remediating their invasions (Gardener et al. 2012GARDENER M, BUSTAMANTE RO, HERRERA I, DURIGAN G, PIVELLO VR, MORO MF, STOLL A, LANGDON B, BARUCH Z, RICO A, ARREDONDO-NUÑEZ A & FLORES S. 2012. Plant invasions research in Latin America: Fast track to a more focused agenda. Plant Ecol Divers 5: 225-232.).

There was no variation in the students’ knowledge from both municipalities regarding exotic species and, consequently, no effect concerning the presence of the CUF upon such knowledge. Such a scenario may be related to the fact that there were no environmental education projects occurring in that conservation unit before or even when we performed our research. Therefore, only the presence of the CUF is not enough to influence the students’ knowledge regarding the topic we studied. We also observed that there were no educational projects in both municipalities concerning biological invasions. In light of this, we suggest developing environmental educational projects relating to biological invasions that effectively educate schools, and the local community are developed.

Students living in rural or urban areas share similar knowledge of exotic species. This is related to the small difference between the urbanization degree of rural and urban areas in both municipalities, which corresponded to small-sized cities located in the state’s countryside. Additionally, the students’ knowledge was similar, despite different frequencies of contact with nature, which may be related to the anthropization and environmental degradation present in the surroundings of both municipalities. Such features may be making it difficult for the students to visualize and have contact with native species. Finally, we also observed that practical classes and visitation to the CUF did not influence the students’ knowledge, which may be related to the low quality and/or frequency of such activities in the school visits from both municipalities.

Students’ limited capacity to identify native species from exotic species shows their limited knowledge of Brazilian fauna’s common and local representatives and that they are distant/disconnected from their surrounding natural environments (Beatley 2011BEATLEY T. 2011. Biophilic cities: The importance of nature and wildness in our urban lives. Washington, DC: Island Press.). Lately, the experiences people have with nature are considerably low when compared to older generations (Louv 2005LOUV R. 2005. Last child in the woods: Saving our children from nature-deficit disorder. Chapel Hill, NC: Algonquin Books of Chapel Hill.), with children spending much more time inside their homes in front of different types of screens (e.g., television, computers, smartphones, tablets). In the long term, children’s reduced knowledge of their surrounding biodiversity may start a cycle of disaffection, degradation, and distancing these individuals towards nature that may cause more biodiversity losses without being perceived as prejudicial (Pyle 2003PYLE RM. 2003. Nature matrix: Reconnecting people and nature. Oryx 37: 206-214.). Such disconnection across generations makes people apathetic to a depauperated and eroded biodiversity, a vague reference of natural environments that can negatively affect establishing practical conservation goals by stakeholders (Miller 2005MILLER JR. 2005. Biodiversity conservation and the extinction of experience. Trends Ecol Evol 20: 430-434., Pauly 2004PAULY D. 2004. Anecdotes and the shifting baseline. Trends Ecol Evol 10: 430.). These results agree with those observed by Bizerril (2004)BIZERRIL MXA. 2004. Children’s perceptions of Brazilian Cerrado landscapes and biodiversity. J Environ Educ 35: 47-58., who showed that individuals that attained low identification rates of exotic species also had unfamiliarity with native biodiversity from the Brazilian Cerrado Savanna. Considering this Brazilian biome, it is found that in both municipalities of this research, it is one of the world’s to 25 biodiversity hotspots (Myers et al. 2000MYERS N, MITTERMEIER RA, MITTERMEIER CG, DA FONSECA GAB & KENT J. 2000. Biodiversity hotspots for conservation priorities. Nature 403: 853-858.), such unfamiliarity with local biodiversity is even more worrisome. An approach aiming for better dissemination and understanding of the Cerrado’s biodiversity for primary-school and high school students may result in students identifying more with its native species, creating and enforcing their connection with nature and, eventually, contributing to its conservation (Bizerril 2004BIZERRIL MXA. 2004. Children’s perceptions of Brazilian Cerrado landscapes and biodiversity. J Environ Educ 35: 47-58.).

The majority of the species cited to be primarily conserved were large-bodied species, mainly mammals, which shows the students’ attachment and preference for some taxa, mostly charismatic animals, as shown before (Ballouard et al. 2011BALLOUARD JM, BRISCHOUX F & BONNET X. 2011. Children prioritize virtual exotic biodiversity over local biodiversity. PLoS One 6: e23152., Genovart et al. 2013GENOVART M, TAVECCHIA G, ENSEÑAT JJ & LAIOLO P. 2013. Holding up a mirror to the society: Children recognize exotic species much more than local ones. Biol Conserv 159: 484-489., Snaddon et al. 2008SNADDON JL, TURNER EC & FOSTER WA. 2008. Children’s perceptions of rainforest biodiversity: Which animals have the lion’s share of environmental awareness? PLoS One 3: e2579.). More extensive media coverage about these species may be one reason for such a tendency to choose more prominent and popular ones. Such excessive preference for some species is likely to contribute to neglect and decreased conservation efforts for small-bodied and less emblematic taxa, such as invertebrates, reptiles, amphibians, fishes, and plants (Clucas et al. 2008CLUCAS B, MCHUGH K & CARO T. 2008. Flagship species on covers of US conservation and nature magazines. Biodiver Conserv 17: 1517-1528., Randler et al. 2012RANDLER C, HUMMEL E & PROKOP P. 2012. Practical work at school reduces disgust and fear of unpopular animals. Soc Anim J Human-Animal Stud 20: 61-74.).

Although the students were able to rank 118 native species to be primarily conserved, this number only represents 3% of all animal species threatened to extinction and listed in the Red List of Threatened Species from the International Union for the Conservation of Nature. The low number of endangered species cited and identified as threatened by the students is in stark contrast to the students’ capacity of learning and recognition of up to 493 Pokemon species, along with their “ecological” and “functional” attributes, as shown previously (e.g., Balmford et al. 2002BALMFORD A, CLEGG L, COULSON T & TAYLOR J. 2002. Why conservationists should heed Pokémon. Science 295: 2367-2367.). Therefore, if children and teenagers are appropriately encouraged and stimulated, educational conservation actions towards better control, remediation, and exotic species management may be significantly improved, mostly if this is done in more interesting ways (Balmford et al. 2002BALMFORD A, CLEGG L, COULSON T & TAYLOR J. 2002. Why conservationists should heed Pokémon. Science 295: 2367-2367.).

According to Wilson’s (1984)WILSON EO. 1984. Biophilia: The human bond with other species. Harvard University Press, Cambridge. biophilia theory, interactions with nature satisfy human beings’ innate impulses to connect with nature. Other studies already verified that contact with nature increases human well-being, resulting in better psychological and physiological benefits (Mayer et al. 2009MAYER FS, FRANTZ CMP, BRUEHLMAN-SENECAL E & DOLLIVER K. 2009. Why is nature beneficial? The role of connectedness to nature. Environ Behav 41: 607-643., Zelenski et al. 2015ZELENSKI JM, DOPKO RL & CAPALDI CA. 2015. Cooperation is in our nature: Nature exposure may promote cooperative and environmentally sustainable behavior. J Environ Psychol 42: 24-31.). Different methodologies may be developed within schools to involve students with natural environments and, consequently, native species. For instance, making use of recreational and outdoor education, ecological trails, parks, CUF visitations, or even green spaces in urban areas that are available for visitation may improve and reinforce the connection of the students with nature (Huckauf 2005HUCKAUF A. 2005. Biodiversity conservation and the extinction of experience. Trends Ecol Evol 20: 430-434.). These methods contradict the traditional and formal school environments, usually characterized by an exhaustive and non-interactive learning environment (Abreu et al. 2017ABREU J, SOUSA JW & LACERDA M. 2017. Um aplicativo móvel para educação ambiental. Brazilian Symp Comput Educ 28: 1736-1738.). Consequently, if applied, these other perspectives may allow the students a better understanding of biological and ecological elements and components (Echeverría 2015ECHEVERRÍA JA. 2015. A escola contínua e o trabalho no espaço-tempo eletrônico. In: Jarauta B & Imbernón F (Eds), Pensando no futuro da educação: Uma nova escola para o século XXII, p. 37-60.).

Citizen science is an alternative for improving students’ perception of native species in addition to involving the active participation of the community to produce scientific data and stimulate interest in the conservation of species (Bonney et al. 2009BONNEY R, COOPER CB, DICKINSON J, KELLING S, PHILLIPS T, ROSENBERG KV & SHIRK J. 2009. Citizen science: A developing tool for expanding science knowledge and scientific literacy. BioScience 59: 977-984., Cohn 2008COHN JP. 2008. Citizen science : Can volunteers do real research? BioScience 58: 192-197., Dickinson et al. 2012DICKINSON JL, SHIRK J, BONTER D, BONNEY R, CRAIN RL, MARTIN J, PHILLIPS T & PURCELL K. 2012. The current state of citizen science as a tool for ecological research and public engagement. Front Ecol Environ 10: 291-297., Lewandowski & Oberhauser 2015LEWANDOWSKI EJ & OBERHAUSER KS. 2015. Butterfly citizen scientists in the United States increase their engagement in conservation. Biol Conserv 208: 106-112., Sullivan et al. 2009SULLIVAN BL, WOOD CL, ILIFF MJ, BONNEY RE, FINK D & KELLING S. 2009. eBird: A citizen-based bird observation network in the biological sciences. Biol Conserv 142: 2282-2292.). Combining ecological research with environmental education through citizen science may cause positive learning results in the students’ and the public’s general biological and environmental education and improve exotic species’ management (Dickinson et al. 2012DICKINSON JL, SHIRK J, BONTER D, BONNEY R, CRAIN RL, MARTIN J, PHILLIPS T & PURCELL K. 2012. The current state of citizen science as a tool for ecological research and public engagement. Front Ecol Environ 10: 291-297.).

Still, implementing better teaching practices in Brazil is challenging, given the country’s current education system. The scant educational resources, allied with the expected budget cuts that Brazilian science is currently facing (Dobrovolski et al. 2018DOBROVOLSKI R, LOYOLA R, RATTIS L, GOUVEIA SF, CARDOSO D, SANTOS-SILVA R, GONÇALVES-SOUZA D, BINI LM & DINIZ-FILHO JAF. 2018. Science and democracy must orientate Brazil’s path to sustainability. Perspect Ecol Conserv 16: 121-124., Escobar 2015ESCOBAR H. 2015. Fiscal crisis has Brazilian scientists scrambling. Science 349: 909-910., Fearnside 2016FEARNSIDE PM. 2016. Brazilian politics threaten environmental policies. Science 353: 746-748., Wade 2016WADE L. 2016. Brazilian crisis threatens science and environment. Science 352: 1044.) constitute an imminent increase to the already deficient educational, cultural, and scientific differences across the different regions of the country. Nonetheless, considering the availability of several methodologies mentioned above, we believe that even in a low availability of resources, it is still possible to improve students’ education and learning to popularize topics related to exotic and native species.

ACKNOWLEDGMENTS

We thank João Carlos Nabout, Solange Xavier, Paulo De Marco Júnior, Mirley Santos, and Rebecca Dew for suggesting changes to the manuscript. We thank the schools’ directors and teachers for participating in our research. Finally, we thank the employees from FLONA for their receptivity during the data sampling. EPCM thanks Universidade Estadual de Goiás for the graduate scholarship (Bolsa de Pós-Graduação Stricto Sensu) and the students’ mobility aid provided from the agreement UEG/CAPES Nº 817164/2015. This study was financed in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior – Brazil (CAPES). DPS and RPB received productivity grant from Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq, proc. numbers: 304494/2019-4 and 309894/2017-4, respectively). The authors declare there is no conflict of interests.

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Publication Dates

  • Publication in this collection
    18 Jan 2021
  • Date of issue
    2021

History

  • Received
    2 Dec 2019
  • Accepted
    15 June 2020
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