Integrating Different Types of Knowledge to Understand Temporal Changes in Reef Landscapes

Abstract

Reefs are highly diverse ecosystems threatened by anthropogenic actions that change their structure and dynamics. Many of these changes have been witnessed by different reef users who hold specific knowledge about the reefscape according to their experiences and uses. We aimed to understand whether fishers, divers, and reef scientists have different perceptions of general changes that have occurred in reefs and whether their knowledge converge, diverge or are complementary. We conducted 172 semi-structured interviews with stakeholders from Northeast and Southeast Brazil where either coral or rocky reefs occur, comprising most reefs occurring in the Southwestern Atlantic Ocean. Reef scientists and divers perceived corals have undergone the sharpest declines among reef species and indicate pollution and tourism as the major negative impacts on reefs. On the contrary, fishers noticed greater declines in fishing targets (i.e., groupers) and have hardly noticed differences in coral abundance or diversity over time. Divers had a broader view of changes in reef organisms, with some level of convergence with both reef scientists and fishers, while reef scientists and fishers provided information on more specific groups and economically relevant resources, respectively. The different stakeholders generally agree that reefscapes have undergone negative changes including diversity loss and abundance declines of reef organisms. The complementarity of information among different stakeholders enables a better understanding of how human behavior impact and perceive changes in natural ecosystems, which could be essential to manage reef environments, particularly those without baseline data.

Full text

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ORIGINAL RESEARCH
published: 08 November 2021
doi: 10.3389/fevo.2021.709414
Edited by:
Rômulo Romeu Nóbrega Alves,
State University of Paraíba, Brazil
Reviewed by:
Ian C. Enochs,
Atlantic Oceanographic
and Meteorological Laboratory
(NOAA), United States
Vinicius J. Giglio,
Federal University of São Paulo, Brazil
*Correspondence:
Maria Iohara Quirino-Amador
iohara.quirino@gmail.com
Specialty section:
This article was submitted to
Conservation and Restoration
Ecology,
a section of the journal
Frontiers in Ecology and Evolution
Received: 13 May 2021
Accepted: 15 October 2021
Published: 08 November 2021
Citation:
Quirino-Amador MI, Longo GO,
Freire FAdM and Lopes PFM (2021)
Integrating Different Types
of Knowledge to Understand
Temporal Changes in Reef
Landscapes.
Front. Ecol. Evol. 9:709414.
doi: 10.3389/fevo.2021.709414
Integrating Different Types of
Knowledge to Understand Temporal
Changes in Reef Landscapes
Maria Iohara Quirino-Amador1,2*, Guilherme Ortigara Longo1,3 ,
Fúlvio Aurélio de Morais Freire1,4 and Priscila F. M. Lopes1,2
1Programa de Pós-graduação em Ecologia, Centro de Biociências, Universidade Federal do Rio Grande do Norte, Natal,
Brazil, 2Fishing, Ecology, Management and Economics (FEME), Department of Ecology, Universidade Federal do Rio Grande
do Norte, Natal, Brazil, 3Marine Ecology Laboratory, Department of Oceanography and Limnology, Universidade Federal do
Rio Grande do Norte, Natal, Brazil, 4Laboratory of Ecology and Evolution of Crustaceans (LABEEC), Department of Botany
and Zoology, Universidade Federal do Rio Grande do Norte, Natal, Brazil
Reefs are highly diverse ecosystems threatened by anthropogenic actions that change
their structure and dynamics. Many of these changes have been witnessed by different
reef users who hold specific knowledge about the reefscape according to their
experiences and uses. We aimed to understand whether fishers, divers, and reef
scientists have different perceptions of general changes that have occurred in reefs and
whether their knowledge converge, diverge or are complementary. We conducted 172
semi-structured interviews with stakeholders from Northeast and Southeast Brazil where
either coral or rocky reefs occur, comprising most reefs occurring in the Southwestern
Atlantic Ocean. Reef scientists and divers perceived corals have undergone the
sharpest declines among reef species and indicate pollution and tourism as the major
negative impacts on reefs. On the contrary, fishers noticed greater declines in fishing
targets (i.e., groupers) and have hardly noticed differences in coral abundance or
diversity over time. Divers had a broader view of changes in reef organisms, with
some level of convergence with both reef scientists and fishers, while reef scientists
and fishers provided information on more specific groups and economically relevant
resources, respectively. The different stakeholders generally agree that reefscapes have
undergone negative changes including diversity loss and abundance declines of reef
organisms. The complementarity of information among different stakeholders enables a
better understanding of how human behavior impact and perceive changes in natural
ecosystems, which could be essential to manage reef environments, particularly those
without baseline data.
Keywords: stakeholder perceptions, Brazilian reefs, environmental perception, random forest, Southwestern
Atlantic reefs, recreational divers, artisanal fishers, marine scientists
INTRODUCTION
Humans have depended on coastal reef resources for millennia (Cinner et al., 2018). The
dependency and interactions between people and reefs (i.e., economic and cultural) may vary
greatly over time, within and among social groups. Certain groups of people may be more
dependent on reefs than others, which may also vary through time or seasonally (Costanza, 1999).
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The interactions between human populations and reefscapes
happen through different stakeholders (Marshall et al., 2018), for
example, institutional agents responsible for ordering reef use,
non-governmental organizations that focus on reef conservation,
reef scientists interested in understanding how reefs work, and
people that make direct use (extractive or not) of reefs, such as
fishers, tourism operators, diving companies, and tourists.
These stakeholders may have different and/or complementary
perceptions of the reefs depending on the type and frequency
of their use (Eddy et al., 2018). Regular users can pay attention
to different characteristics of these environments depending on
how they use and access them, which would explain why people
have contrasting memories of changes in natural environments
(Hicks et al., 2013). For example, there is strong evidence that
fishers have detailed knowledge about temporal changes in their
target species (Johannes et al., 2000) but do not notice declines in
species with less or none economic importance (Damasio et al.,
2015). Divers may perceive differences in biological attributes
such as fish richness and coral cover, as well as in the structural
complexity of coral reefs (Uyarra et al., 2009) and scientists may
restrict their perceptions to their particular study target (e.g.,
fishes or corals).
Reconciling knowledge from different stakeholders, of variable
age groups and experiences is an alternative to reconstruct the
process of change that a particular species or environment gone
through (Hansen et al., 2006). This could be an important
tool to reconstruct sensitive reefscapes in areas that lack
baseline data and struggle with research funding, management,
and enforcement. This is the case of Southwestern Atlantic
reefs, most of which are within Brazilian territory, occurring
between the latitudes ∼5◦N and 27◦S and are marked by
high species endemism of corals and fishes (Leão et al., 2016;
Francini-Filho et al., 2018). These reefs are not homogeneous
(Aued et al., 2018), while some of them are similar to typical
coral reefs (Northeast region), others consist of rocky reefs
that can support coral assemblages (Southeast and South
regions; Leão et al., 2003). Brazilian reefs are found in
shallow margins close to the coast, island edges and isolated
banks (Leão et al., 2003;Kikuchi et al., 2010), many of
them are close to densely populated areas where they are
more subjected to direct anthropogenic impacts (Moura, 2000;
Magris et al., 2021). Brazilian reefs are generally used for
both extractive (i.e., fishing) and non-extractive activities (i.e.,
tourism, recreational diving, and scientific research), and these
uses are often more intense when reefs are closer to the
shore. Fishing, climate changes and pollution are among the
main threats to Brazilian marine biodiversity (Magris et al.,
2021), which combined may have caused severe changes in
reef biodiversity.
We aimed to understand whether fishers, recreational divers,
and reef scientists who use Brazilian reefs have a different
perception about potential changes these reefs have undergone
and whether they tend to converge or diverge on specific
aspects of change. By unraveling, recognizing and connecting
these perceptions we may be able to produce a more accurate
historical reconstruction of changes and their magnitude in
these ecosystems.
MATERIALS AND METHODS
This study was conducted between June 2018 and October 2019
in seven states along 3,133 km of the Brazilian coast (Figure 1), an
area that comprises more than 50% of the distribution of reefs and
diverse reef structures in Northeast and Southeast Brazil (Leão
et al., 2016;Aued et al., 2018). The interview procedures were
approved by the Ethics Committee at the Federal University of
Rio Grande do Norte (CAAE: 73739917.3.0000.5537) and, in the
case of protected areas, by the Brazilian System for Authorization
and Information on Biodiversity (SISBIO: 65379).
Interviewed Stakeholders
We interviewed the stakeholders who make direct and constant
use of reefs, namely fishers, recreational divers, and reef scientists.
Among fishers, we focused on those who practice spearfishing
to ensure a closer contact with the reefs, although we eventually
included some fishers who use gillnets and hook-and-line,
provided they were specialists in reef fishing. Despite not having a
daily contact with reefs, recreational divers tend to have a unique
and contemplative view of reefscapes because of the cultural
values attributed to this leisure activity (Arin and Kramer,
2002), therefore we interviewed recreational divers and diving
instructors. Among reef scientists, we focused on those whose
research is focused on understanding reef ecological processes
as we were interested in observable changes in living organisms.
Despite our effort to find individuals within each of these groups
of stakeholders (fishers, divers, and scientists) in every state we
visited, we were unable to include representatives from all three
categories in all states, either for logistical reasons and/or ease of
access to certain groups. For example, in the state of Paraíba, we
were only able to interview divers (Figure 1).
Data Collection
First, we identified key informants as leaders of fishing
organizations, diving companies and recreational divers, and
acquainted professors at universities known to at least one of the
authors. From this initial list, we used the “snowball” technique,
in which the key informants indicated people who they deemed
relevant to contribute with the requested information (Goodman,
1961). These new informants named successive ones until we
exhausted names or our capacity to reach them. Opportunistic
interviews were also conducted with stakeholders who fit the
criteria to answer the questionnaire. All interviewees exclusively
answered about the reefs locations they had experience with
throughout their lives. The interviews were conducted in two
ways: in-person and using online forms. The online form was
mainly used to reach divers, although some reef scientists also
used this platform due to the difficulty of arranging face-to-
face meetings.
The questionnaire was divided in three sessions (Table 1):
“Personal data and impressions” in which we collected
information on stakeholders’ age, experience, reef region,
among others; “Historical knowledge” in which we were
interested in identifying the stakeholders’ perception of
organisms that decreased or increased in reef landscapes;
and “Abiotic environment and threats” in which we asked
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FIGURE 1 | States, where stakeholders were interviewed, are highlighted and divided between the region where coral reefs (states in darker blue) and rocky reefs
(states in light blue) are found. It is shown which stakeholders were interviewed in each state: fishers with a sailboat, divers represented with a snorkel, and reef
scientists symbolized with a hand glass. The map on the bottom left showing South America, localizing Brazil.
interviewees about changes in water and climate, how they
perceived the pollution, and impacts in reef landscapes. We
included in the questionnaires organisms that are conspicuous
to the benthic (Aued et al., 2018) and fish communities (Morais
et al., 2017), and that are perceived to be more subject to
changes (Supplementary Table 1). We presented photographs
of these organisms to the interviewees so that they could inform
whether they knew the species and whether they had noticed
changes in their abundance. Respondents were also free to list
other species or groups of organisms for which they noticed
changes in abundance. All data will be available upon reasonable
request to the authors.
Data Analysis
In order to assess the agreement between and within the groups
of stakeholders we combined three analytical methods: Random
Forest (RF), Permutational Analysis of Variance (PERMANOVA)
and Non-metric Multidimensional Scaling (NMDS). The RF
is a supervised learning algorithm (James et al., 2013) that
randomly creates a forest, combining decision trees to obtain
predictions with greater accuracy and stability (James et al.,
2013). The RF was used herein for two main purposes: (1) to
understand how the different variables contribute to define a
group of stakeholders (i.e., perceiving changes in abundance
in a specific group) through the accuracy and Gini value; and
(2) to assess how cohesive each stakeholder group is in their
perceptions through a confusion matrix. The accuracy and Gini
indicators designate which variables define the groups (fishers,
divers, and reef scientists). The confusion matrix is obtained
using the “out-of-bag” forecast for each observation in the
training set of trees (Cutler et al., 2012). The variables with the
highest number of mentions by stakeholders in each category
(two models: decrease and increase) were chosen to compose
the RF model (Table 1). All variables contained in the “Abiotic
environment and threats” component and the “Environmental
health” variable were used for the characteristics of the “Abiotic
environment and impressions” block (Table 1). PERMANOVA
and nMDS were used to test and visualize the groups formed
by organisms which have decreased and organisms that have
increased (Table 1). The PERMANOVA was used to assess if
the dispersion of the stakeholders’ responses is different among
the three groups (Anderson, 2017). The nMDS based on Jaccard
distances was used to visualize the outputs of the RF allowing to
assess the qualitative interrelationships between the variables and
to define which variables were most related to each stakeholder
group. The number of axes in the nMDS was chosen to maintain
the stress value below 0.15 and ensure that any existing patterns in
the data would be captured by the multidimensional ordination
space. All analyzes were performed using the RStudio v interface
1.2.5033, an integrated development environment for R program
(R Core Team, 2019), using the “randomForest” (Liaw and
Wiener, 2002), “factoextra” (Kassambara and Mundt, 2017),
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TABLE 1 | Variables used in the study organized into three different components with their description, types, and analyses performed.
Components Groups and variables Description Variables types Analysis
Personal data and impressions Stakeholder Type of stakeholder. “Fisher”; “Diver,” and “Reef
scientists”
Nominal Descriptive
Age Stakeholder’s age (years) Discrete Descriptive
Experience How long the stakeholders have been engaged
in research, fishing, or diving (years)
Discrete Descriptive
Initial and final contact Years of initial and final contact with the chosen
reef environment (year)
Discrete Descriptive
Environmental health Regards the first and last contact with the
environment, evaluated in the following
categories: excellent; good; median; bad; and
terrible. Divided into two categories: “initial
health” and “recent health”
Ordinal Random Forest
Historical knowledge Organism decrease Species the stakeholders noticed which have
decreased in the reef environment
Nominal Descriptive
Organism decrease groups Number of mentions per stakeholder for each
category of organisms that have decreased It
includes the following variables: “Massive
corals,” “Branched corals,” “Echinoderm,”
“Cartilaginous fish,” “Epinephelidae fish”
(groupers), “Labridae fish: Scarinae” (parrotfish),
“Other reef groups,” “Mollusks,” and
“Crustaceans”
Discrete Random Forest and
NMDS
PERMANOVA
Organism increase Species that the stakeholders noticed that have
increased in the reef environment
Nominal Descriptive
Organism increase groups Number of mentions per stakeholder for each
category of organisms that have increased
Includes the following: “other reef groups,”
“Invasive,” “Zoanthids,” “Echinoderm,”
“Pomacentridae Fish” (damselfish), and “Algae”
Discrete Random Forest,
NMDS, and
PERMANOVA
New organisms Exotic and invasive species Nominal Descriptive
Abiotic environment and threats Water Assessment of reef water turbidity: “More
turbid”; "Less turbid"; and "The same”
Ordinal Random Forest
Climate Changes that have occurred in the regional
climate (open response)
Nominal Random Forest
Pollution Perception of pollution of the reef environment:
“More polluted”; “Less polluted”; and “The
same”
Ordinal Random Forest
Impacts The three main threats to reef landscapes in
order of importance
Nominal Random Forest
“FactoMineR” (Lê et al., 2008), “vegan” (Oksanen et al., 2019),
“ggplot2” (Wickham, 2016), “grid” (R Core Team, 2019), and
“ggrepel” packages (Slowikowski, 2019).
RESULTS
Stakeholders’ Profile
Fishers
Fishers formed the oldest (average = 49 yo) and most experienced
group of respondents (∼33 years of career; Table 2), providing
approximately six decades of perceptions about the changes
in Brazilian reefs. Most of them were spearfishers (71.0%),
although some fished with gillnets (20.2%), and hook-and-
line (8.7%). Fishers made 297 citations of organisms that they
perceived as having declined (Table 2), but 29 of them were
disregarded as they did not refer to species necessarily dependent
on reefs (i.e., manatees). Likewise, six mentions of organisms
that fishers perceived as having increased were disregarded for
referring to cetaceans.
Among the organisms perceived by fishers to have
decreased, the most cited groups were parrotfish (“Labridae:
Scarinae,” 36.1% of the fishers citations), followed by groupers
(“Epinephelinae,” 52.1%), sharks and rays (“Cartilaginous,”
55.95% of fishers citations; Figure 2A). Among the organisms
perceived to have increased, sea turtles stood out with 64.6%
of the citations (Figure 2B). Only nine fishers mentioned the
presence of new organisms, which exclusively referred to the
sun coral (Tubastraea spp.). Most fishers said they believe
reefs became more polluted (56.5%) and more turbid (68.1%)
in comparison to the beginning of their career. About 55%
also noticed changes in the local climate over their years of
experience. Fishers also indicate industrial fishing as the main
threat to reefs.
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TABLE 2 | Main qualitative results according to the interviewed stakeholders (fishers, reef scientists, and divers).
Fishers Divers Reef scientists
No. of interviews 69 60 43
Age (with standard deviation) 49 years (mean)
25 to 75 years ( ±10.2)
35 years (mean)
21to54(±8.6)
45 years (mean)
24 to 80 years ( ±13.0)
Experience (with standard deviation) 33 years (mean)
10 to 63 years ( ±12.2)
15 years (mean)
1 to 42 years ( ±11.08)
20 years (mean)
4 to 48 years ( ±12.01)
Organisms that decreased (citations) 297
(4.3 per person)
336
(5.6 per person)
213
(5 per person)
Organisms that increased (citations) 126
(1.8 per person)
78
(1.3 per person)
107
(2.8 per person)
Reef threats (main answers %) Industrial fishing (44.9)
Tourism (17.4)
Divines reasons (14.5)
Climate change (55.9)
Pollution (48.3)
Tourism (33.3)
Fishing (27.5)
Tourism (27.5)
Pollution (22.5)
Pollution % (more polluted) 56.5 68.3 74.4
Water % (more turbid) 68.1 35 37.2
Climate change % (noticed any change) 33.3 43.7 20.9
Environmental health – beginning (main answers %) Great (72.5)
Good (11.6)
Great (45)
Good (38.3)
Intermediate (51.2)
Good (30.2)
Environmental health – currently (main answers %) Bad (46.4)
Horrible (43.5)
Intermediate (38.3)
Bad (35)
Intermediate (53.4)
Bad (27.9)
Divers
Divers formed the youngest and least experienced group (35
years old, 15 years of experience, on average), but even so, they
were the ones who cited the highest number of organisms that
have declined (N= 336; Table 2). Similar to other stakeholders,
divers highlighted the decline of “Massive corals” (55.31% of
divers’ citations) followed by parrotfish (“Labridae: Scarinae”;
42.6%), (Figure 2A). On the other hand, divers also noticed
an increase in damselfish (“Pomacentridae”; 37.9% of divers’
citations), “Zoanthids” (34.8%) and “Algae” (27.2%) (Figure 2B).
Divers also indicated the appearance of new organisms, with 11
mentions of the sun coral (Tubastraea spp.) and six mentions
of other organisms including algae, mollusks, and the lionfish
(Pterois volitans). Most divers believe that water turbidity (65%)
and climate (56.3%) have not changed since the beginning of their
experiences in the past decades. On the other hand, most divers
suggested that the reef environment became more polluted,
sustain an intermediate health status (Table 2), and indicate
climate change as the major threat to reefs.
Reef Scientists
Reef scientists were on average 45 years old and a maximum of
20 years of experience (Table 2). Similar to fishers, reef scientists
also noticed declines of parrotfish (“Labridae: Scarinae”; 21.3%
of the reef scientists’ citations), and “Massive corals” (42.5%)
(Figure 2A). They also noticed an increase in “Sea turtles” (24.4%
of citations) and “Zoanthids” (46.5%) (Figure 2B). Ten reef
scientists (23.2%) also noticed the presence of new organisms
in the reef landscapes, especially the sun coral (Tubastraea spp.;
10 mentions). The other new organisms mentioned (N= 14)
included octocoral species, ascidians, lionfish (P. volitans),
sponges, the polychaeta Branchioma spp. and the ophiuroid
Ophiothela spp. Most reef scientists (74.4%) suggested that reefs
are now more polluted and some of them (37.2%) indicated that
the water is more turbid in comparison the beginning of their
careers. Most of them also chose not to give their opinion on
the impact of climate changes on reefscapes. Reef scientists see
fishing as the main threat to reefs and have more conservative
opinions on general reef health classifying it as intermediate but
stable since the beginning of their careers (Table 2).
Agreement Among Stakeholders
The three groups of stakeholders share a general perception that
the reef health has deteriorated over time. About 46% of fishers
classified the current reef health as “bad,” 53.4% of reef scientists
and 38.3% of divers classified as “intermediate” (Table 2).
Regarding the general and abiotic aspects of perception (first
random forest analysis), the three groups of stakeholders differ
in how they evaluate the “Initial health,” “Recent health,” and the
“Impacts” sources (Random Forest: accuracy 63.4%) (Figure 3A).
Divers and reef scientists showed less homogeneous responses
within each group, with 50% and 34% being mistakenly classified
as belonging to another group of stakeholders, respectively
(Supplementary Table 2). Most fishers were recognized as such
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FIGURE 2 | Main organisms mentioned by fishers, divers, and reef scientists as having decreased (A) or increased (B) in the Brazilian reef landscapes in the last six
decades. Only organisms that had a minimum of 5% in each group of citations were included among the total citations of increase and decrease, respectively. The
down arrow on the left represents the organisms that declined, and the up arrow on the right represents the organisms that increased in reef landscapes.
(74%), 21.7% were recognized as divers, and 4.3% as reef
scientists. About 50% of the divers were recognized as such,
26.6% as fishers and 23.3% as reef scientists. Among the reef
scientists, 65.1% were recognized as such and 27.9% as divers
(Supplementary Table 2).
Regarding the species that stakeholders perceive to have
declined (second random forest analysis), their main differences
were on the groups “Massive Corals” and “Epinephelidae Fish”
(Random Forest: 63.4% accuracy; Figure 3B). The fact that
fishers mostly perceive decreases in fish-related organisms, such
as parrotfishes and groupers made them significantly different
from the other stakeholders (PERMANOVA p-adjusted (0.003;
Supplementary Table 3), who tended to mention massive corals
more often (Supplementary Tables 2,3). Reef scientists were
highly mixed with the other stakeholders in the Random Forest:
53.5% were identified as divers and 13.9% as fishers. Specifically,
most fishers were recognized as such, but 18.8% were recognized
as divers. Most divers were also identified as belonging to their
own group, however, 18.3% were recognized as fishers and 15%
as reef scientists (Supplementary Table 2). These trends were
confirmed by the nMDS analysis, which showed that fishers
tended to mention more “Cartilaginous Fish” and “Epinephelidae
Fish” compared to the other stakeholders (Figure 4A). In turn,
reef scientists and divers tended to mention “Massive corals,”
“Echinoderm,” and “Branched corals” (Figure 4A).
The most important factors separating the stakeholders for
species which were perceived as having increased are “other
reef groups,” “Invasive” and “Echinoderm” groups (Random
Forest: accuracy 59.9%) (Figure 3C). In this case, all groups
of stakeholders were significantly different from each other
(Supplementary Table 3). Again, reef scientists were the
least recognized stakeholders by the model: only 39.5% were
recognized as such, 46.5% were characterized as divers, and
13.9% as fishers, reinforcing the dispersion of information among
these stakeholders (Supplementary Table 2). Most fishers and
divers were identified as such, except for 37.7% of the fishers
who were recognized as divers, and 25% of the divers who were
characterized as fishers. In this specific nMDS, fishers were more
associated through citations of “Sea turtle” groups, while reef
scientists and divers were more associated to the citation of
“Zoanthids” and “Invasive” groups (Figure 4B).
DISCUSSION
The three groups of stakeholders perceived changes in reef health
and pollution, generally agreeing that many species declined
in abundance. Because these groups had different perceptions
regarding which species have declined or increased, combining
their knowledge can help create a more comprehensive
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FIGURE 3 | Random Forest accuracy and Gini values showing the main variables responsible for the differences in stakeholder perception on. (A) Changes in abiotic
reef environment. (B) Organisms that have decreased. (C) Organisms that have increased in reef landscapes. Notice that the higher the accuracy or the Gini value,
the more likely it is that that variable contributed to separating the stakeholders according to their perceptions.
understanding of past changes in Southwestern Atlantic reefs.
Stakeholders noticed changes in organisms related to their
occupations. For instance, fishers mentioned decreases in
targeted fishes, such as parrotfish, groupers, sharks and rays,
including multiple species that have been overfished and in dire
need of management (Giglio et al., 2014;Lessa et al., 2016;
Roos et al., 2020). They also indicated a great decrease in
shark species within the genus Sphyrna spp. and particularly the
species Ginglymostoma cirratum between the 1980s and 1990s
(Leduc et al., 2021), and in the locally important black grouper
Mycteroperca bonaci (Bender et al., 2014). Parrotfish decline have
started in the 1990s, although the exploitation of some species,
such as Scarus trispinosus, may have started in the mid-1980s
in some parts of the country (Bender et al., 2014). Divers and
reef scientists noticed coral declines more frequently than fishers
probably because they are more likely to pay attention to the
reef substrate and sessile invertebrates due to their recreational
and scientific interest, respectively (Giglio et al., 2015). This
perception is corroborated by the increase in coral mortality due
to more frequent and intense thermal anomalies in addition to
land-based stressors in Brazil (Teixeira et al., 2021). Reef scientists
were also the only stakeholder group to notice a decline in sea
urchin populations. Interestingly, fishers reported an increase in
the abundance of black urchins. Sea urchin declines were largely
documented in the Atlantic Ocean, such as the emblematic case
of Diadema antillarum that almost disappeared after a massive
die-off caused by a disease in 1983–1984, which is linked to
increased algal abundance in many Caribbean reefs (Hughes,
1994;Tuya et al., 2005). However, such decline noticed by
scientists in Brazil probably had little to know effect on sea urchin
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FIGURE 4 | Non-metric multidimensional scaling (NMDS) for organisms that have change in reef landscapes comparing the perception of the three types of
stakeholders in the study: fishers, divers, and reef scientists. (A) Organisms that have declined (“stress value” = 0.12). (B) Organisms that have increased (“stress
value” = 0.07). The stakeholders are represented through the colorful vectors, purple for fishers, red for divers, and blue for reef scientists. The black vectors
represented the trend data for three types of stakeholders.
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Quirino-Amador et al. Stakeholder Knowledge About Reef Changes
herbivory since current abundances seem to be enough to control
macroalgal in shallow zones of subtropical reefs (Cordeiro et al.,
2020). Stakeholders also have different perceptions on which
organisms have increased in Southwestern Atlantic reefs. Divers
mentioned the increase of organisms in shallow coastal reefs (i.e.,
Pomacentridae fish, zoanthids, and algae), an area often used
by diving companies. Illegal feeding to attract fish and entertain
tourists in some of these areas (Silva et al., 2020) may also have
affected their perception of increase in abundance. Reef scientists
mentioned reef organisms that increased but that were not on
the original list (e.g., sponges) and were the only stakeholder
group to spontaneously classify a species as invasive. Fishers
mentioned an increase in sea turtle abundance more often than
any other group of stakeholders, which may be directly related
to a fishing ban established in the early 1990’s (Marcovaldi and
Marcovaldi, 1999) and to the numerous reports of bycatch in
gillnets (Marcovaldi et al., 2006), increasing the contact between
fishers and sea turtles. The recovery in sea turtle populations
can also be attributed to a massive protection of sea turtle nests
in Brazil for over 30 years (Marcovaldi and Chaloupka, 2007).
Mentions of new organisms was rare regardless of the stakeholder
group, but when it occurred the sun coral Tubastraea spp. was
the most cited organism. There is evidence that Tubastraea spp.
have been spreading throughout Brazilian reefs, from the states
of Ceará (3◦S) to Santa Catarina (∼27◦S), being a major problem
in rocky reefs of Southeastern Brazil (Riul et al., 2013;Capel et al.,
2019). Indeed, the sun coral may significantly change the reef
community, since experimental competitive interactions between
the invasive Tubastraea tagusensis and the native coral Siderastrea
stellata caused significant damaged and mortality in the native
species (Miranda et al., 2016).
Fishers were generally more pessimistic about the current
health state of reefs, which may be related to the decline in stocks
of their fishing targets, but also to the fact that they use reefs and
the oceans more often than any other user. Divers also classified
the current reef health as “bad,” which is likely due to their greater
contact with touristic sites, which tend to be more degraded
compared to those far from the coast (Hannak et al., 2011). Reef
scientists were relatively more optimistic classifying reef health as
“intermediate” or “bad.” Although it is not possible to state the
reason for this difference in perception among stakeholders, reef
scientists use external references from the literature in addition to
personal experiences to assess the health status of Brazilian reefs.
Therefore, these unified opinions of reef health among scientists
may exist because of their education and experience, that could
even compensate the shifting baseline because of their formal
knowledge (Muldrow et al., 2020). In addition, reef scientists are
divers with scientific training and experience, and often interact
with fishers or assess information provided by fishers (Bender
et al., 2013), which could explain why their perception was mixed
with those groups of stakeholder.
Different stakeholders also attributed different threats to the
reefs that would help explain their current health status. We
only interviewed artisanal fishers and they cited industrial fishing
as an important impact on reefs. However, reefs are mainly
fished by artisanal fishing, and some of its gear can indeed
damage corals (Link et al., 2019) and cause significant impact to
fish stocks (Bender et al., 2014). Denying that artisanal fishing
activities can have negative consequences to reefs can hinder
decision-making (Vaclavikova et al., 2011). For example, fishers
may resist management measures, even those aimed at protecting
endangered species, if they do not feel at least partially responsible
for current reef health. Some fishers also highlighted that impacts
on reefs happen for divine reasons, which suggests the difficulty
and need to bring scientific information to these groups (Hilborn,
2007). Reef scientists also highlighted the negative impacts of
fishing activity on reefs, specifically causing overfishing. Part
of these reef scientists may be more aware of the impact of
fisheries for being part of groups that assist the government in
designing fishing regulations, so they may have access to more
detailed fisheries information on a national level. These scientists
are invited to these groups exactly for their expertise on the
species and awareness of the stock status, these groups facilitate
the exchange of information increasing their understanding of
fishing impacts.
All groups perceived some level of negative impact of tourism
on reefs, which is widely recognized in the literature (Giglio
et al., 2017, 2020). Reef scientists are likely to deal with or
be aware of impacts caused by tourism such as fish feeding,
coral removal, and over-visitation (Liu et al., 2012). Fishers may
have a conflict with tourism activities, including competition
over space use (Outeiro et al., 2019). Divers may be especially
aware of the impact of tourism because they are directly related
to this activity (Neto et al., 2017), some of them are tour
guides in reef environments and/or have great contact with
tourism companies that often give or receive instructions to avoid
their impacts on reefs. The fact that some divers understand
the impacts of tourism, despite working in or promoting
the sector, possibly suggests that they have been following
reef degradation in areas increasingly subjected to visitation
(Dearden et al., 2007). Conversely, divers can also be critical
allies of science and conservation through their involvement in
citizen-science programs that suggest divers without previous
scientific training can provide reliable estimates of fish abundance
(Vieira et al., 2020).
The increase in pollution was also perceived by most
stakeholders, although especially by reef scientists and divers,
who are more likely to visually notice it in reefs (Costa, 2007).
Only divers rated climate change as the most important factor
among reef threats. Perhaps divers are more exposed to this
type of information through the media and social media than
fishers, who tend to have low education levels and poor access
to other social services. Divers are also possibly less afraid of
expressing an unsupported opinion than reef scientists who do
not work on climate-related issues. Scientists are experts in
their specialism and expect to be recognized for it, which is
probably why scientists do not want to express opinions about
subjects outside their expertise (Myers, 2003). In fact, not even
the consecutive cases of bleaching observed on the Brazilian coast
(Dias and Gondim, 2016;Leão et al., 2019;Ferreira et al., 2021)
seem to have been enough to make climate change an important
issue to be raised here by reef scientists. A possible factor for this
is the lower frequency of thermal anomalies in South Atlantic and
particularly low post-bleaching mortality (<5%) when compared
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Quirino-Amador et al. Stakeholder Knowledge About Reef Changes
to the Pacific and Caribbean until recently (Mies et al., 2020).
Climate change may also be difficult to be perceived on its own,
especially when it is not easily associated to local climate events
(Spence et al., 2011).
Overall, fishers provided more consistent responses. The
interviewed fishers were precisely those who target species similar
to the fish presented in the questionnaire. Fishers may also be
immersed in a more culturally homogeneous world in small
coastal communities than that shared by reef scientists and divers
from different regions of the country (Reis and D’Incao, 2000).
Unlike fishers, reef scientists have their specific interests diffused
over a large set of reef species. Compared to the other stakeholder
groups, reef scientists provided the least homogeneous responses,
sometimes confused with those of fishers, but mainly with
those of divers. Although many reef scientists are attentive to
interspecific relationships, most are focused on particular groups
of organisms and their opinions may only lean toward their
research object.
Different stakeholder groups agreed with the changes in reef
landscapes, but also share conflicting notions on specific subjects.
This disagreement can represent an obstacle to governance and
the management of natural resources (Yandle, 2003;Suárez de
Vivero et al., 2008), but can also be a source of complementarity
as each group perceive unique aspects of changes on ecosystems.
Converging information reinforces the idea that some species or
certain abiotic characteristics have undergone significant changes
that are noticeable by all. By combining these perceptions, we
gathered strong evidence that parrotfishes, groupers, sharks, and
corals have undergone significant declines, whereas seaweeds,
zoanthids and damselfishes have increased in Brazilian reefs.
Pollution and fishing are major problems and reef health has
suffered and overall decline. Such a scenario may jeopardize
not only reef biodiversity but the benefit it provides to many
people that depend on it for multiple uses. Combining different
knowledge is an important step toward understanding the history
of human-caused impacts on ecosystems, mitigating impacts,
restoring key ecosystem functions, and preparing for the future.
DATA AVAILABILITY STATEMENT
The raw data supporting the conclusions of this article will be
made available by the authors, without undue reservation.
ETHICS STATEMENT
The studies involving human participants were reviewed and
approved by the Ethics Committee at the Federal University
of Rio Grande do Norte (CAAE: 73739917.3.0000.5537)
and Brazilian System for Authorization and Information on
Biodiversity (SISBIO: 65379), with the latter specifically for
research done in protected areas. Written informed consent for
participation was not required for this study in accordance with
the National Legislation and the Institutional Requirements.
AUTHOR CONTRIBUTIONS
MQ-A and GL conceived the idea and developed it with
PL. MQ-A collected all the data. PL and GL contacted key
participants for the interviews. MQ-A and FF performed the
statistical analyses. MQ-A and PL wrote the manuscript with
inputs from all co-authors and also designed the figures. All
authors contributed with text revision and the final format
of the manuscript.
FUNDING
This study was partially financed by the Coordenação de
Aperfeiçoamento de Pessoal de Nível Superior – Brasil (CAPES) –
Finance Code 001 through a master’s scholarship awarded to
MQ-A. This study was supported by Serrapilheira Institute with
a grant awarded to GL (Serra-1708-15364).
ACKNOWLEDGMENTS
PL and GL thank the National Council for Scientific and
Technological Development (CNPq) for a research productivity
grants (301515/2019-0 and 310517/2019-2, respectively). We
thank the Brazilian Citizen Science project “#DeOlhoNosCorais”
supported by Serrapilheira Institute (R-1805-24275 awarded to
GL) for helping promote the study and collect online data,
and Júlia Gonçalves for the manuscript’s illustrations. Finally,
we also thank all the fishers, divers, and reef scientists for
their contribution.
SUPPLEMENTARY MATERIAL
The Supplementary Material for this article can be found
online at: https://www.frontiersin.org/articles/10.3389/fevo.2021.
709414/full#supplementary-material
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Frontiers in Ecology and Evolution | www.frontiersin.org 12 November 2021 | Volume 9 | Article 709414