Concern has been raised about the effects of artisanal and recreational fishing on the size and abundance of coastal fishes (McClenachan 2009a; Costello et al. 2012). Conventional model-based assessments are commonly undertaken by state research and management agencies as a standard to determine the status of artisanal and recreational fishing effort and stock abundance. This kind of assessment relies on monitoring or fisheries-dependent data (Prince and Hordyk 2019), which in many cases are absent, not fully reliable, or too recent to detect fish population changes that may have occurred decades ago (Eero and MacKenzie 2011; Sadovy et al. 2020). As a result, regulatory action in many low- and middle-income countries is frequently delayed or nonexistent (Worm and Branch 2012; Young et al. 2014; Dowling et al. 2016; Fitzgerald et al. 2018).
In data-poor contexts, assessments based on systematized fishers' memories (Ainsworth et al. 2008; Young et al. 2014; Thurstan et al. 2016), photographs (McClenachan 2009b; Jiménez-Alvarado et al. 2019), and other historical documents (Young et al. 2015) are critical to understanding the status of fisheries and driving regulatory action. Evidence shows that neglecting historical sources of information for assessment may have a direct negative impact on fisheries management (Moffitt et al. 2010) and could result in the normalization of highly reduced fish abundances and the setting of lower recovery targets or fishing quotas that would be too high if historical data were considered (McClenachan et al. 2012). Therefore, it is key to include fishers' local ecological knowledge (LEK) and other sources of historical information in the reconstruction of fish catches and indicators (Bender et al. 2014).
The term “local ecological knowledge” refers to a body of knowledge, both individually acquired and shared through generations, that is based on the practical experience of and observations by users (Braga-Pereira et al. 2022). It is often based on long-term and recurrent observations of a particular ecosystem, considering patterns, variations, and interactions between species and their habitats (Ruddle 2000; Deshpande et al. 2019). Local ecological knowledge constitutes one of the most versatile and transcendental sources of historical information and has already been used to assess species biodiversity, abundance, and population trends across different taxa and environments (Anadón et al. 2010; Thurstan et al. 2015). In marine environments, LEK has been widely used to support management and monitoring of biodiversity, ecological dynamics, and fisheries (e.g., Olsson and Folke 2001; Moller et al. 2004; Hind 2015; Kroloff et al. 2019). For instance, it has helped to understand the causes and effects of Bonefish Albula vulpes decline in south Florida, United States (Kroloff et al. 2019); to assess population trends of data-poor finfish species over the period 1950–2007 in the Philippines (Lavides et al. 2009); to evaluate changes in spatial recreational fishing patterns from 1950 to 2010 in Puget Sound, United States (Beaudreau and Whitney 2016); to estimate illegal fishing in territorial user rights for fisheries systems in Chile (Romero et al. 2022); and to assess the decline of several fish species in southeastern Brazil (Bender et al. 2014), as well as several other examples (e.g., Close and Hall 2006; Ruddle and Hickey 2008; Taylor et al. 2011; Loerzel et al. 2017; Zapelini et al. 2017). The ability of LEK to provide relevant and reliable information for management has been proven to be increasingly useful over the past decades, and its adoption to complement conventional assessments has been repeatedly recommended to agencies (Huntington 2000; Olsson and Folke 2001; Davis and Wagner 2003; Gilchrist et al. 2005; Anadón et al. 2009; Lavides et al. 2009; Thornton et al. 2010; Daw et al. 2011; Hind 2015; Beaudreau and Whitney 2016; Kroloff et al. 2019).
To strengthen natural resource management, LEK can be structured as expert knowledge to fill information gaps (Steele and Shackleton 2010; Braga and Schiavetti 2013). The extent to which this knowledge is effectively used largely depends on the methodological approach—specifically, how it can reduce the inherent biases of expert knowledge and produce robust estimations of indicators that are relevant, representative, and comparable within the respective field (Tversky and Kahneman 1974; Burgman 2016). For this, it is necessary to rely on systematic expert elicitation processes (Davis and Wagner 2003).
In this study, we designed and implemented an expert elicitation process to gather LEK on coastal fisheries exploitation patterns from artisanal and recreational spearfishers. We specifically assessed trends in catch composition and the geographical distribution of the catch for a selected group of data-poor coastal groundfish of Peru. Insights on management measures for these fisheries and the further use of LEK and alternative assessment methods are discussed.
METHODS Spatial frameworkSpatially, the Peruvian coastline was divided into three biogeographical regions corresponding to north, central, and south (Figure 1). These biogeographical regions were only used for our specific research purpose (i.e., not official designations) and were based on an adapted version of the “most updated” zoning system proposed by Marín Soto et al. (2017). The modification was to merge the north zone and the tropical north zone into one region (north) because the tropical north would comprise too small of an area alone and because, in terms of the fish species composition reported by the divers interviewed in this study, both regions were similar and clearly different from the central region.
FIGURE 1. Fishing grounds (numbered key) and delimitation of biogeographical regions (red lines) of the Peruvian coastline. The brown boundary delimits Peru's territorial waters.
The Peruvian coastline was also divided into 27 fishing grounds (Figure 1) by applying the following principles based on our previous knowledge and preliminary expert consultations: (1) traditional recognition, meaning that the divers considered each one of the fishing grounds to be a relatable and recognizable unit despite having many “fishing spots” within; (2) internal similarity, in terms of the types of habitats, environmental conditions, and species traditionally recognized as present in the area that make a fishing ground a unit despite the variable size; and (3) external difference, which was based on the same criteria as principle 2 but with regard to the clearly identifiable differences between grounds. We aimed to achieve the best degree of local detail without burdening the experts too much by making the interviews too long and tedious or by asking for a level of detail that was outside their scope of remembrance. Accordingly, fishing ground sizes were highly variable. This is particularly evident in the northern region between fishing grounds 4 and 6, where the convergence zone between the Peru Coastal Current and the Ecuador–Peru Coastal Current occurs (Barahona et al. 2019), displaying a gradual but recognizable change in environmental conditions and species composition.
Species selection and methodological approachPeruvian commercial and recreational spearfishing, performed while free diving, started in the early 1950s, when a few families based in Callao (location included in fishing ground 17) and Pucusana (fishing ground 20; Figure 1), mostly of Italian descent, produced the first homemade pieces of equipment (Mustiga 2006). Since then, spearfishing has grown along with other small-scale coastal fisheries operating with various gears but having common target species, and it has expanded across the entire coastline.
Based on our previous knowledge, expert recommendations, and the analysis of regulatory framework and available data, we composed a list of 10 unassessed and data-poor coastal groundfish species to be evaluated in this study. These species are seldom part of landing statistics—mostly due to a low reporting frequency from fishers and the common use of unofficial landing sites and because they do not appear to make a great contribution in terms of catch volumes or gross revenue. The list includes mostly shallow-water reef fish: the Harlequin Wrasse Bodianus eclancheri, Galapagos Sheephead Wrasse Semicossyphus darwini, Chino Medialuna ancietae, Pacific Beakfish Oplegnathus insignis, Negrillo Graus nigra, Pacific Goliath Grouper Epinephelus quinquefasciatus, and Bumphead Parrotfish Scarus perrico. It also includes the following: the Grape-eye Seabass Hemilutjanus macrophthalmos, which behaves as a shallow-water reef fish in the southern and central regions of Peru but can reach greater depths in the northern tip of the country; the Broomtail Grouper Mycteroperca xenarcha, for which the main distribution comprises the northern region and a part of the central region of Peru, and which behaves mostly as a shallow-water reef fish but can reportedly be caught at deeper reefs in particular areas and around oil rigs (only in the north); and the Black Snook Centropomus nigrescens, which has a super-shallow distribution that is associated not only with reefs, but also with sandbars.
Based on expert consultation, we know that the first seven species listed above are caught mainly by spearfishing, either while free diving or with the use of hookah gear, and their vertical distribution almost completely overlaps with free-diving ranges (0–30 m); this applies to Grape-eye Seabass in the southern and central regions as well. The Grape-eye Seabass is also targeted by a bottom longline fishery in northern Peru. The Broomtail Grouper is also subject to (1) very small bottom trolling and handline commercial fisheries, which operate mainly off the coastlines of Lobitos, Cabo Blanco, El Ñuro, and Los Órganos from 5 to 210 m depth (Tullio Chapillequén, Ángel Calderón, and Javier Mogollón, personal communication); and (2) handline fisheries operating off Cancas and Punta Mero, which predominantly catch the species in and around reefs at depths between 15 and 20 m (Solange Alemán, personal communication). Finally, the Black Snook is also targeted by small commercial and recreational fisheries employing coastal gill nets and fishing rods. In this last case, the seasonally turbid waters along the shores at the northern tip of Peru might reduce the frequency of divers encountering this species, but the turbidity was constant throughout the study years and the vertical overlap was complete. The interaction of other fisheries for these same species, such as the fisheries operating with coastal gill nets or purse seines in shallow-water areas, was deemed to be limited. Therefore, the information provided by spearfishers in this study was considered representative of the trends and dynamics of the species' populations in general.
These species share one or more of the following key features: (1) they are crucial to the food security and local economy of coastal communities; (2) they are endemic to the Humboldt Current ecosystem and small areas of the Galapagos Islands (i.e., Chino, Negrillo, Harlequin Wrasse, and Galapagos Sheephead Wrasse); (3) they have an important ecological role (e.g., Bumphead Parrotfish; Gobalet 2018); and (4) they present biological features that increase their intrinsic vulnerability to fishing (e.g., Broomtail Grouper, Pacific Goliath Grouper, and Grape-eye Seabass; Araya et al. 2018; Abas 2019). In fact, the Galapagos Sheephead Wrasse, Negrillo, and Chino have already shown signs of depletion in neighboring Chile based on evaluations that included both fisheries-dependent data and historical sources of information (Godoy et al. 2010; Araya et al. 2018).
To better understand the status of selected species, we aimed to develop indicators that could reflect abundance and/or resource availability, that have been used to assess data-poor fisheries in other parts of the world, and that could be built based on LEK. We used FishPath, a decision support tool developed by the Science for Nature and People Partnership working group on data-limited fisheries (Dowling et al. 2016), to explore the potential approaches and indicators available and to select the models with the best fit. We identified two data-limited stock assessments defined as a “single indicator based on expert judgment”: (1) changes in the species composition of the catch and (2) changes in the geographical distribution of the catch. These assessments consider changes in an indicator over time and encompass a simple analysis of whatever empirical indicator is available. Changes in the species composition of the catch can reflect specific targeting, demand, environmental, and/or ecological changes. This indicator is particularly applicable to multispecies fisheries, either alone or in a multi-indicator framework, and can be used to define a control rule that responds to a broad shift, which may reflect either changes in fishing behavior or changes in stock status. Changes in the geographical distribution of the catch can reflect the discovery of new fishing grounds, sequential overfishing of existing fishing grounds (serial depletion), or environmental/ecological changes unrelated to fishing (The Nature Conservancy 2022). The process that we followed to gather and use LEK data as input into these assessments is described in detail below.
Sampling approachWe planned and conducted a total of 40 interviews ranging from 2 to 6 h each, depending on the number of combinations of decades and fishing grounds that the spearfishers were able to give information about. Each interview was conducted on at least one date and up to a maximum of four different dates, allowing a slow and conscientious reflection on every response. All interviews were conducted between March and November 2020.
The interviewees were selected based on a main criterion of representativity by applying three principles. The first was the level of experience: we aimed to have an even number of divers that started spearfishing in the decades of 1960–1969, 1970–1979, 1980–1989, 1990–1999, 2000–2009, and 2010–2019 (hereafter, referred to as the 1960s, 1970s, 1980s, etc.), with each category comprising between five and seven people (years of experience ranged from 5 to 30 among the selected divers). These are considered adequate numbers for expert group work (Hanea et al. 2022). The second principle was the type of extraction and included even representation of both commercial and recreational spearfishers. During the selection process, we learned that a large portion of divers who recognized themselves as recreational spearfishers or participated in championships also spearfished commercially on a regular basis. This was particularly true for divers that started between the 1960s and the 1990s, but it held for some younger divers as well. The last principle was geographical representation: we divided the list into three groups and tried to evenly include divers that recognized themselves as local or as having a wide and consistent experience of spearfishing in the northern, central, and southern regions. We also learned during the selection process that Peruvian spearfishers have a long tradition of traveling across the country for spearfishing competitions and commercial and leisure fishing trips, so most of them were able to give information about two or even three regions. The controls that were implemented to avoid biased results based on limited experiences are described in later sections. This provided robustness to the analysis, as we were able to get many more answers than expected for each decade × fishing ground combination.
Based on our accumulated knowledge of this fishery across the coastline, we used social networks and direct contacts within fishing associations and clubs to spread the announcement about this study, including the criteria for selection of interviewees.
Data gatheringTo identify the composition of the average catch during a particular decade and at a particular fishing ground, we designed structured interviews and conducted them using the conferencing platform Zoom. Whenever we learned from our first contact (usually a phone call) that a diver did not have access to Zoom or did not know how to use Zoom, we facilitated the process by getting them help from a friend or relative. At the beginning of each interview, we conducted a “prospection” phase in which we confirmed the diver's level of experience and selected every decade × fishing ground combination for which they could provide information (see survey formats with instructions in “ProspectionFormat_Ground&Decades.xlsx”; Supplementary Material available separately online). We employed Zoom's “share screen” feature using Google Earth to show the diver which fishing spots were included in every fishing ground, visually defining their geographical limits and validating them. We offered historical cues (e.g., president in office at the time, reference to renowned spearfishing competitions that took place in Peru) to help them locate their activities in time. During this phase, we excluded every decade × fishing ground combination for which the diver's experience was reduced to only a few dives (namely, only two 2-day spearfishing contests or only a couple of trips). In principle, only the responses of divers that could recall dives in different years and seasons for a certain decade × fishing ground combination were included in the study.
We asked spearfishers to picture themselves having just gone in from a dive at a certain fishing ground (out of the 27 fishing grounds into which the Peruvian coastline was divided; Figure 1) during a certain decade (i.e., 1960s, 1970s, 1980s, 1990s, 2000s, or 2010s). We then asked them to picture their “normal, regular, day-to-day, average” catch from 1 day of spearfishing and to describe it in terms of the species composition and the number of individuals caught per species. We emphasized the need to include all species that were taken on a regular basis (not only the largest or the most valuable) and to exclude the ones with highly anecdotal occurrence (namely, the extremely rare species for the fishing ground or species whose presence responded specifically to a particular season in a certain year during a climate event, such as a strong El Niño). We stressed the necessity to describe a catch that would represent an average catch of every decade × fishing ground combination, considering the entire range of recalled catches. We specifically avoided mentioning the species listed for evaluation, both before and during the interview, to preclude an unintentional influence over the interviewee's answers.
In this process, sometimes the spearfishers identified a significant change in catch within a decade or a disparity in terms of species composition and abundance between different spots within a fishing ground. When such difficulties were encountered, we asked the spearfishers to mentally average those components to produce an answer that would be representative of the decade and fishing ground. We recognized that this could be difficult and error inducing. To reduce biases, we guided the diver in the process of remembering exactly when (within the decade) and where (inside each fishing ground) they spearfished and what the catches' compositions and numbers were. After this, they could locate themselves better in space and time, remembering, for example, contexts and other divers that were involved. This was very helpful, as it provided the diver with a clearer memory on a range of good and bad catches as well as good and bad ocean conditions. By the end of this sequence, the diver had to mentally average the results of that recall process to provide a description of the catch that would be representative of the decade and fishing ground.
During the interviews, most of the spearfishers provided only common names of fish. We used Zoom's “share screen” feature, searched for all possible species on FishBase (
When a species' identity or the number of reported fish in the catch seemed off or raised doubts based on the latest reports in a certain fishing ground, we requested the divers share historical photographic records and provide further detail. This helped us to identify outliers and to exert a control measure over divers' biases. In total, 275 pieces of historical photographic records were gathered to assess and confirm reports (Figure 2).
FIGURE 2. Four examples of the 275 photographs used to confirm “odd” historical catches along the Peruvian coastline, either by species identity or number of fish caught, reported by spearfishers during the interviews: (A) Galapagos Sheephead Wrasses, Negrillos, Pacific Beakfish, and Chinos caught in Huarmey in 1969 (photo source: Juani Pastorelli); (B) Pacific Goliath Groupers caught in Punta Mero in 1964 (photo source: Ana María Gallia Paredes); (C) multi-color Harlequin Wrasses caught in Cabo Blanco in 1992 (photo source: Alfonso Chávez); and (D) Chinos caught in Marcona in 1982 (photo source: Manuel Milla).
We produced three indicators from the data: species participation index (PI), average daily catch (DC), and species richness in the catch (SR). The PI is the catch proportion of a certain species relative to the total catch; it was obtained by dividing the number of fish of one species that was caught by a certain spearfisher in a certain decade × fishing ground combination by the total number of fish caught by that spearfisher in that decade × fishing ground combination. The DC is the number of fish of a certain species that was caught by one spearfisher in one fishing day and was calculated by averaging all of the direct answers to the question asked. In a similar trend to how changes in catch per unit effort (CPUE) in a fishery is interpreted, changes in the DC may also reflect changes in fish abundance. The SR is the total number of species present in the catch in a certain decade at a certain fishing ground and was obtained by accounting for all species identities that were present in all answers for a particular decade × fishing ground combination. We analyzed the trends of the selected species based on the PI and DC among the three biogeographical regions. To assess changes in the importance of the selected species within the catch, we performed generalized linear models (family: Gaussian) using the decade as the predictive variable and an indicator variable (PI, DC, or SR) as the response variable (α = 0.05). For the PI and DC, we also calculated the order of magnitude of the change if there was any change.
We also estimated the coastline length of every fishing ground (including the perimeter of islands) using ArcGIS version 10.8.1 and calculated the total coastline length for which every selected species was present in the average catch, based on the answer of at least one spearfisher, during a certain decade. Based on this, we calculated the magnitude of change in the coastal length for which every selected species was present in the habitual catch across decades, paying attention to the geographical development of such change. For this analysis, we summed the coastline lengths (m) of all areas where the species was reported by at least one spearfisher in the habitual catch of every decade.
We explored the resulting indicators for evidence of overfishing and sequential depletion after discussing and ruling out other conditions or elements that might have driven changes in the catch composition and the geographical distribution of the catch. In the present study, signs of overfishing are argued to exist whenever the DC of a certain species is consistently and significantly reduced over time, especially if it drops to zero and remains at zero through the end of the timeline (Constantine 2002). Signs of sequential depletion, on the other hand, are explored based on two different but related criteria: (1) whenever the species shows a geographically progressive disappearance from the habitual catch, usually with a clear directionality identified (Clark 1999; Roberts 2002; Berkes et al. 2006; Morsan 2007); or (2) whenever, in a certain fishing ground, the species' relative participation is consistently and significantly reduced while being replaced with other species in the average catch (Link 2007). Both criteria imply an adaptation of the fisheries to the depletion of a species in a fishing ground, either by changing the target species or by progressively changing the fishing ground.
RESULTS Changes in species composition and richness in the catchAt a coastwide level, the PI of all selected species combined showed a significant decrease across the timeline of the study (b = −8.431 × 10−4, t = −12.58, p < 0.001). The trend, however, showed that the PI of the combined selected species peaked somewhere between the 1970s and 1980s before plummeting until the 2010s (Figure 3).
FIGURE 3. Coastwide participation index in the catch (all selected species combined) within coastal waters of Peru across the time span of the study. Shaded ribbon is the 95% confidence interval of the generalized linear model.
When analyzed by biogeographical region, the combined selected species showed a significant decrease in participation within the catch (i.e., PI) for the northern (b = −0.0010354, t = −5.495, p < 0.001), central (b = −7.198 × 10−4, t = −11.8, p < 0.001), and southern (b = −0.0015636, t = −5.559, p < 0.001) regions of Peru. At the species level, although most species showed generally negative trends (Figure 4), some had consistently decreasing curves (i.e., Harlequin Wrasse, Black Snook, Pacific Goliath Grouper, and Broomtail Grouper in the north; Grape-eye Seabass, Chino, and Galapagos Sheephead Wrasse in the central region; Galapagos Sheephead Wrasse in the south), whereas others exhibited peaks of participation around the 1970s, 1980s, and 1990s before decreasing toward the end of the timeline (i.e., Pacific Beakfish in the north; Harlequin Wrasse, Broomtail Grouper, and Pacific Beakfish in the central region; Chino, Grape-eye Seabass, and Pacific Beakfish in the south). Several species exhibited relatively stable PI (i.e., Bumphead Parrotfish in the north; Negrillo in the south). Data for the fishing grounds in the northern region were only consistently available from the 1970s and onward, as spearfishing started later there compared to the central and southern regions of the country.
FIGURE 4. Participation index in the catch for selected species in the (A) northern, (B) central, and (C) southern regions of the Peruvian coastline across the time span of the study.
The SR showed statistically significant increases across the timeline of the study in the northern (b = 0.5, t = 3.918, p < 0.05; Figure 5A) and southern (b = 0.13, t = 3.038, p < 0.05; Figure 5C) regions but not in the central region (b = 0.16, t = 1.076, p = 0.343; Figure 5B). In the north, the SR significantly increased between the 1970s and 1990s and then was relatively stable afterwards, with even a slight decrease between the 2000s and the 2010s (Figure 5A). A similar trend was observed in the south, where the SR increased between the 1960s and 1980s and then stabilized (Figure 5C). In those regions, the catch was dominated by a few high-value prevalent species at the beginning of the timeline (mostly the species evaluated in this study). The decrease in their PI (as shown in Figure 4) was coupled with an increase in the diversity of species habitually caught. In the central region, on the other hand, the diversification trend was present only between the 1960s and 1980s, followed by a short period of stability and a decline in the SR between the 1990s and 2010s. In every case, but more strongly in the northern and central regions, the high-value species (mainly the evaluated ones) that were prevalent at the beginning of the timeline were gradually replaced by other species that were less valuable but more abundant.
FIGURE 5. Species richness in the catch per decade in coastal waters of Peru over the timeline of the study. Shaded ribbon is the 95% confidence interval of the generalized linear model.
The coastwide DC also showed a significant decrease across the timeline of the study (b = −0.02443, t = −19.73, p < 0.001) when all of the selected species were combined. The coastwide DC in the 2010s was one-tenth of the DC in the 1960s with all species combined (Figure 6).
FIGURE 6. Coastwide average daily catch (all selected species pooled) expressed in number of fish caught per diver per day in coastal waters of Peru across the time span of the study. Shaded ribbon is the 95% confidence interval of the generalized linear model.
When analyzed by biogeographical region, the combined selected species also showed a significant decrease in DC for the northern (b = −0.0026988, t = −10.53, p < 0.001), central (b = −0.02144, t = −14.49, p < 0.001), and southern (b = −0.038918, t = −8.096, p < 0.001) regions (Figure 7). Some species showed declines in their DCs across the study timeline. For example, the DC of Pacific Beakfish in the 2010s was roughly 5% and 10% of the historical highest DC in the northern and central regions, respectively. Moreover, in the central region, Grape-eye Seabass and Galapagos Sheephead Wrasse had DCs of more than 1 fish/person/day as their historical highest and Chino had a DC of more than 2 fish/person/day, whereas all three species had DCs of zero or close to zero in the 2010s. The DC of Galapagos Sheephead Wrasse in the southern region during the 2010s was slightly lower than 5% of its historical high value.
FIGURE 7. Average daily catch expressed in number of fish caught per diver per day for selected species in the (A) northern, (B) central, and (C) southern regions of the Peruvian coastline across the time span of the study.
The geographical distribution of target species in the catch changed throughout the time span under analysis. Table 1 summarizes the percentage reduction in the coastline length related to each species' presence in the habitual catch; the coastal length during the decade in which the species had its widest and narrowest distribution in the habitual catch was used as a reference. The Harlequin Wrasse disappeared from the habitual catch in almost every fishing ground where it was once present, only remaining in Hormigas de Afuera, a tiny group of islands and reefs located 62 km offshore from Lima. On the other hand, the Pacific Goliath Grouper disappeared entirely from the habitual catch in Peru. Another species that experienced a clear change was the Galapagos Sheephead Wrasse, which was present in the habitual catch of 14 fishing grounds across the three biogeographical regions during the 1980s. After that, it sequentially decreased from north to south until it was only present in the habitual catch of two fishing grounds in the southern region, comprising a 79.98% reduction in its geographical distribution.
TABLE 1 Changes in geographical distribution of selected species over time based on the maximum and minimum distribution of their catches. Fishing grounds 1–27 are depicted in Figure 1. C, central region; N, northern region; S, southern region.
Selected species | Characteristics associated with maximum distribution | Characteristics associated with minimum distribution | Reduction in coastline length | |||||||
Decade | Coastline length (km) | Number of fishing grounds | N–S fishing ground limits | Decade | Coastline length (km) | Number of fishing grounds | N–S fishing ground limits | Kilometers | Percentage | |
Harlequin Wrasse | 1980s | 860 | 6 | 7 (N) to 22 (S) | 2010s | 2 | 1 | Only in 16 (C) | 859 | 100 |
Black Snooka | 1990s | 241 | 4 | 1 (N) to 4 (N) | 2010s | 196 | 2 | 1 (N) to 2 (N) | 45 | 19 |
Pacific Goliath Grouper | 1980s | 284 | 5 | 1 (N) to 8 (N) | 2010s | 0 | 0 | Absent from habitual catch | 284 | 100 |
Negrillo | 1980s | 1190 | 5 | 22 (C) to 26 (S) | 2010s | 724 | 3 | 23 (S) to 25 (S) | 466 | 39 |
Grape-eye Seabass | 1980s | 1769 | 13 | 16 (C) to 26 (S) | 2010s | 557 | 2 | 22 (C) to 23 (S) | 1212 | 69 |
Chino | 1990s | 2323 | 17 | 7 (N) to 26 (S) | 2010s | 724 | 3 | 22 (S) to 25 (S) | 1599 | 69 |
Broomtail Grouper | 1980s | 1311 | 12 | 1 (N) to 22 (C) | 2010s | 673 | 7 | 1 (N) to 16 (C) | 638 | 49 |
Pacific Beakfish | 1980s | 2456 | 21 | 1 (N) to 26 (S) | 2010s | 1521 | 13 | 4 (N) to 23 (S) | 936 | 38 |
Galapagos Sheephead Wrasse | 1980s | 2259 | 14 | 7 (N) to 26 (S) | 2010s | 452 | 2 | Only in 23 (S) and 25 (S) | 1807 | 80 |
Bumphead Parrotfishb | 1990s | 265 | 5 | 1 (N) to 5 (N) | 2010s | 241 | 4 | 1 (N) to 4 (N) | 24 | 9 |
aThe maximum coastline calculated for Black Snook excludes the zone of Sechura (fishing ground 7) because its reported catch during the 1970s was based on the answer of only one diver and had a disproportionately strong influence over the outcome due to the size of the fishing ground.
bThe maximum coastline calculated for Bumphead Parrotfish excludes the zone of Sechura (fishing ground 7) because its geographical distribution was temporarily extended south during an El Niño event that occurred in the late 1990s.
Similar patterns were evidenced for the Chino and Grape-eye Seabass. The Chino was found within only three fishing grounds at the end of the timeline, also only in the south, comprising a 68.85% reduction. The Grape-eye Seabass was once present at 13 fishing grounds in the central and southern regions, but at the end of the timeline it was found within only two fishing grounds in the south (a 68.51% reduction). On the other hand, the Negrillo, Broomtail Grouper, and Pacific Beakfish showed reductions of about 38–48% in the geographical distribution of their presence in the habitual catch, while the Black Snook and Bumphead Parrotfish (only present in the northern region across the timeline under analysis) showed lesser reductions of about 8–19%.
DISCUSSION Structured expert elicitation to obtain local ecological knowledgeFisheries management is traditionally supported using conventional model-based assessments. Fisheries that are assessed this way are—with very few exceptions—large in scale, rich in data and research capacities, and considered relatively well managed (Hilborn and Ovando 2014), as high data requirements to execute these kinds of assessments can be met. However, small-scale fisheries that share those characteristics are scarce around the world. In this context, failing to recognize the relevance and validity of other assessment methods and types of data, such as LEK, needlessly causes management paralysis despite warnings of overfishing (Dowling et al. 2016; Prince and Hordyk 2019).
As evidenced by an increasingly high number of studies, LEK can provide high-quality information to support management in data-poor fisheries (Ainsworth et al. 2008; Bender et al. 2014; Young et al. 2014; Thurstan et al. 2016). However, its qualitative and subjective nature poses challenges in its application for stock assessments. Structured expert elicitation processes can provide protocols and control measures to produce LEK-based quantitative estimates that can be statistically analyzed (Martin et al. 2012; McBride et al. 2012).
In this study, LEK was used to produce indicators (PI, DC, and SR) that allowed us to identify trends and dynamics of coastal groundfish populations from direct observations made by experienced spearfishers. This approach allows for the construction of historical baselines that otherwise would be impossible to determine. Local ecological knowledge represents a huge opportunity in the assessment of data-poor fisheries, as major shifts and decreases in populations could have occurred decades ago, before the recording of fisheries or monitoring data was initiated (Myers and Worm 2003). Detecting the existence of this “ski-jump” effect may help to adjust and improve management measures implemented in fisheries that are currently being assessed using relatively recent data (Sadovy et al. 2020).
Like any data collection methodology, expert judgment is subject to error, bias, and uncertainty (Hanea et al. 2022). We applied best practices on expert elicitation methodologies—from a deep understanding of the context, needs, and challenges of the fishery—to facilitate the estimation of uncertain variables (Hemming et al. 2018). We reduced potential biases by applying highly structured framing and limits for the presented question, providing support for historical and geographical situations, clearly communicating the limits of fishing grounds with the help of geographical information system tools, applying controls and checks in each phase of the elicitation process, sharing the survey formats with the interviewees at all times, and avoiding the disclosure of information about the evaluated species and the assessed indicators (e.g., Estévez et al. 2019). One of the most important features of our expert elicitation process was that we did not, in any way, ask about perceptions on the status of the fisheries, the dynamics observed in species' presence, or the possible explanations for the changes that they might have experienced (which many divers felt compelled to provide). We explicitly avoided getting into those discussions and reoriented the interview back to the proposed question. We emphasized the importance of eliminating every idea or hypothesis about the dynamics of the fisheries and just providing an honest and representative answer focusing on the spearfisher's personal memory of the actual catch. This allowed us to reduce biases, as the indicators and models built on the data were not influenced as much by the perceptions or constructs of the divers regarding the addressed issue. This approach adds to the literature on expert elicitation and fisheries, which has generally aimed to obtain an answer to the research question or problem by directly asking the experts to provide an estimation of the indicator or variable. Instead, we obtained the base data and analyzed those data statistically to produce the indicators, as if they were catch data recorded in the field (Van der Fels-Klerx et al. 2005; O'Leary et al. 2009; Adams-Hosking et al. 2016; Hemming et al. 2018; Estévez et al. 2019).
As expected, there were conditions and individual differences between the respondents that inevitably increased the variability of the responses—for example, individual extraction skills and species or technique preferences that varied over the years, time availability, or decreased memory in elder interviewees, among other factors. Some of these caveats should be further addressed by applying additional controls in future applications of similar methodologies.
Status of selected speciesIn the cases of the Harlequin Wrasse, Galapagos Sheephead Wrasse, Chino, Grape-eye Seabass, and Pacific Goliath Grouper, our results suggested a scenario of (1) overfishing based on dramatic reductions in DC down to 0–10% of the historical high value in some regions (Harley et al. 2001; Erisman et al. 2011) and (2) sequential depletion based on a significant reduction or total loss of relative participation in the catch within one or more regions (Link 2007). In addition, significant and progressive decreases of between 60% and 100% in the coastal length comprising the geographical distribution of the species catch were observed (Collen et al. 2016; Dowling et al. 2016). For the Pacific Beakfish and Broomtail Grouper, observed reductions in DC (20% and 25% of the historical high values by the end of the timeline, respectively), decreases in relative participation in the northern (by 24% for Broomtail Grouper) and central (by 13% for Pacific Beakfish) regions, and reductions in the geographical distribution of the catch (38.09% and 48.65%, respectively) also provided evidence of overfishing and sequential depletion but to a lesser degree. Of all species assessed, only the Negrillo, Bumphead Parrotfish, and Black Snook experienced negligible reductions in the geographical distribution of their catch, DC, and relative participation in the catch.
Although there is clearly an interplay between environmental conditions and fishing effort that may explain these trends, evidence from Peru signals an important anthropogenic component. The Peruvian central region is a predominantly subtropical area characterized by cyclical regime changes between colder and warmer periods (Philander 1983; Deser and Wallace 1987; Glynn 1988; Paredes et al. 2004). We have not found evidence that any major unidirectional environmental change occurred between 1960 and 2019 that could have resulted in the drastic reductions of abundance and geographical distribution observed for some of the assessed species. Extreme El Niño events did occur in 1982–1983, 1986–1987, and 1997–1998, with huge impacts on the Peruvian coastline (Hu et al. 2019). These events have been known to produce a change of species composition in the northern and central regions of the country, with a higher occurrence of species typically associated with warmer waters and a lower occurrence of species associated with the Peru Coastal Current (Hooker 1998; Gárate and Pacheco 2004). Based on this information, we would have expected to observe, in the data provided by fishers, an expansion of the presence of Black Snook, Bumphead Parrotfish, Broomtail Grouper, and Pacific Goliath Grouper toward the southernmost part of the northern region and into the central region during both the 1980s and the 1990s. However, this effect was only observed to a very limited extent for the Bumphead Parrotfish. In the 1990s, its reported distribution in the catch extended down to Sechura (fishing ground 7), which is the larger fishing ground of the northern region. In the rest of the decades, the distribution of the Bumphead Parrotfish was mainly stable. The distribution of Broomtail Grouper included fishing grounds down to Paracas (fishing ground 22) at the southernmost end of the central region during the 1960s, but it did not experience an expansion toward the south during the 1990s. In fact, its distribution only shrunk northward during the 1980s and 1990s. The Black Snook also did not show any clear sign of southerly expansion in those decades. The Pacific Goliath Grouper was distributed in three fishing grounds during the 1970s and then expanded to five fishing grounds during the 1980s. However, a clear decrease was observed afterwards: down to two fishing grounds in the 1990s, one fishing ground in the 2000s, and none in the 2010s. We also need to consider the possibility that the southerly expansion observed for some of these species in the 1980s responded to the fact that the spearfishing population experienced a faster growth in the northern region during that decade (Rosendo Mimbela, local spearfisher, personal communication) and started reaching areas that were not previously frequented, such as Isla Lobos de Tierra and Lobitos. Later, these became common spearfishing grounds.
On the other hand, the species associated with the Humboldt Current ecosystem did not show a reduction of their distribution toward the south during the 1980s. On the contrary, for many species, the 1980s was the decade with the wider geographical distribution in their catch. During the 1990s, the distribution of some species (e.g., Galapagos Sheephead Wrasse, Chino, and Grape-eye Seabass) in the catch did experience a retreat toward the south, but in the following decades, they did not recover to the distribution observed during the 1970s or 1980s. Depending on the species, the interplay between fisheries and environmental factors differs and does not show a clear trend that could explain the changes in the assessed indicators.
The groupers (Epinephelidae; Broomtail and Pacific Goliath groupers) and the Humboldt Current endemic wrasses (Labridae; Harlequin and Galapagos Sheephead wrasses) are reportedly threatened or experiencing overfishing worldwide (Sadovy and Eklund 1999; Coleman et al. 2000; Sadovy et al. 2003, 2007, 2011, 2020; Giglio et al. 2014; Sherman et al. 2016; Erisman and Craig 2018; Daly et al. 2020; Khasanah et al. 2020; Arieta 2022). Other Humboldt Current endemic species, such as the Grape-eye Seabass, Chino, and Pacific Beakfish, also showed medium to extremely high levels of reduction in their relative participation within the habitual catch in addition to decreases in the geographical distribution of their catch. Results suggest that many of these species, which were once consistently present in the catch across the country, were progressively cornered into a few areas of southern Peru by the 2010s (see Table 1). For example, the Harlequin Wrasse can now only be consistently found around a couple of small, unpopulated islands located about 62 km offshore from the port of Callao in central Peru. As this species has rarely been reported in Chile (only in the northern tip and mostly during El Niño events; Sielfeld et al. 2002, 2010) and is present in very specific areas of the Galapagos Islands (Edgar et al. 2004; Guarderas Sevilla 2019), a reduction in its occupied habitat for almost the entire Peruvian coast might reflect a critical reduction in its total distribution. The Chino and Galapagos Sheephead Wrasse experienced the largest absolute reduction in their distribution among all the selected species (losses of 1599.33 and 1806.84 km, respectively) and were cornered to only two and three fishing grounds in the south, respectively. The Pacific Goliath Grouper, a species that is particularly vulnerable to fishing due to its life history characteristics (Abas 2019), experienced a reduction of 100% in the geographical distribution of its catch. However, it must be taken into consideration that the Peruvian tropical north comprises the southernmost end of its range (Chirichigno 1974; Heemstra and Randall 1993; Craig et al. 2009), which could produce an occasional influx of individuals when conditions are ideal. In addition to that, the Pacific Goliath Grouper is now only anecdotally reported in fishing grounds that present bad conditions for spearfishing most of the year (e.g., Peña Redonda, Huacura, and Acapulco) due to their proximity to the northern rivers' mouths (e.g., high turbidity), which may also mean that it could be present but is not catchable.
Consistent reductions in the relative participation in the catch of highly valued species and the consequent replacement with other, underappreciated species have been deemed to be a sign of sequential depletion in other case studies (Link 2007), as past experiences have shown that fisheries shift to other species as the primary target species become overexploited. Fishers typically target species that are more abundant as historically high-value fish decline (Brodziak and Link 2002). Notably, the replaced species are all still highly desired by recreational spearfishers and maintain an increasingly high market value, suggesting that the shift responds mainly to changes in availability of the resource rather than a change in the fishery's behavior. For five of the assessed species, changes in the geographical distribution had a sequential component, showing a progressive “retreat” of species presence in the catch toward a few concentrated fishing grounds. Ecological impacts of sequential depletion may result in a reduction of the ecological roles available, with a potential alteration of ecosystem resilience or stability (Gunderson 2000; Fonseca and Ganade 2001; Bellwood et al. 2003; Dıaz et al. 2003; Wohl et al. 2004; Micheli and Halpern 2005; Munari et al. 2005; Essington et al. 2006). In the case of wrasses, this unintended consequence could become serious considering their role in the biological control of populations of urchins that feed on kelp rhizoids (Foster and Schiel 2010; Nichols et al. 2015).
Changes in the SR for this fishery signals a diversification coastwide. At the beginning of the timeline, catch was dominated by a few valuable species that were widely available in fishing grounds that are shallow, highly protected from waves, and easy to access while shore diving. When those species could not be found in such spots anymore, spearfishers started moving toward spots that were rougher, deeper, or only reachable by boat. Other highly valuable species that are usually found in such conditions then started appearing in the catch (elicited spearfishers, personal communications). This was the main reason for Chino and Pacific Beakfish (reported by elicited experts to seek refuge in super-shallow, rough, rocky areas) as well as Grape-eye Seabass (reported by elicited experts to respond to fishing pressure by moving deeper and seeking shelter in rocky caves) to peak in their relative participation within the catch between the 1970s and 1990s. After those decades and considering the nearshore and shallow distribution of these species, spearfishers adapted to their lower availability by targeting a wider range of other, less-valuable fish. Only in the central region, the number of species in the catch reached a plateau and decreased from the 1990s and onward. By the end of the timeline under assessment, the catch composition in the central region was dominated by omnivorous and opportunistic species, such as the Peruvian Morwong Cheilodactylus variegatus and the Peruvian Grunt Anisotremus scapularis (Samamé et al. 1995; Moreno and Flores 2002; Palma and Ojeda 2002; Perez-Matus et al. 2012; Cornejo-Acevedo et al. 2014; Campos-León et al. 2021).
Our results indicate that a significant decrease in abundance, both overall and at the species level, occurred during the decades-long assessed period for 7 of the 10 selected species. The DC can be understood as a simple generic measure of CPUE, with the number of fish caught by a diver (i.e., catch) in one spearfishing day (i.e., effort). The catchability of the species in the spearfishery has not been reduced over the decades because spearfishing equipment is constantly improving, divers are more adapted to rough conditions and deep dives than they were in previous years, and the population of spearfishers is not known to have diminished. In addition, the vertical distribution of the assessed species is mostly in coastal shallow waters. Hence, changes in DC would indicate changes in fish abundance. Accordingly, the cases of the Galapagos Sheephead Wrasse, Chino, and Grape-eye Seabass in the central region were dramatic, as these species had a DC of 1 or 2 fish/person/day in the 1960s and 1970s, which consistently fell toward zero at the end of the timeline. The magnitude of the change in DC for Pacific Beakfish in the central region, Broomtail Grouper in the northern region, and especially Galapagos Sheephead Wrasse in the southern region can be interpreted as a clear sign of overfishing.
These decreasing trends also have a correlation with results of studies showing how the dramatic growth of the Peruvian small-scale fleet and fishing effort in the past few decades has caused a decline in nominal and effective CPUE across various gears within the artisanal fishery (Alfaro-Shigueto et al. 2010; de la Puente et al. 2020). While the highest rate of growth in the small-scale fishing effort occurred from the early 2000s and onward, effort grew consistently starting in the 1950s. Accordingly, we need to consider that nearshore stocks may have experienced the effects of increased effort earlier than others because they were the most accessible at the time when coastal fisheries development started. When fishing near the shore started to show less profitability, vessels intuitively targeted stocks further off the coast. Moreover, nominal CPUE results of the “divers” fleet, which mostly operates with air-compressed hookah systems and targets benthic invertebrates and groundfish in nearshore waters (Marín Soto et al. 2017), describe a remarkably similar trend compared to our results. Both studies show CPUE peaking between the early 1970s and late 1980s, followed by a consistent decrease by the end of the 2010s (de la Puente et al. 2020). Some of the evaluated species responded to fishing pressure by going deeper or inhabiting rocky shores constantly exposed to swell (elicited experts, personal communications). However, this does not account for the observed changes, as the fishery also adapted to those changes and vertical distribution constraints predominantly maintained the fish populations within diving ranges.
Two of the assessed species are caught by other fisheries besides spearfishing, and their cases should be further discussed. The Grape-eye Seabass is considered a southern coastal species that inhabits shallow areas with underwater caves (Cisternas and Sielfeld 2008) in the southern and central regions. However, the species has also been described to have a demersal behavior in deeper areas of the northern region. As such, field experts indicate that the species was targeted by bottom gill-net and longline fisheries from the 1980s to the mid-2000s (Simón Chapillequén, personal communication). Landings data from the Instituto del Mar del Perú, collected by coastal laboratories from 2000 to 2019, showed a peak in 2008 of more than 70 metric tons. From 2011 until the end of the timeline, landings were consistently below 9% of the referred historical maximum, supporting the idea that this stock might have experienced a collapse in the country (Worm et al. 2006). The Broomtail Grouper, on the other hand, is also subject to small bottom trolling and handline fisheries that operate mainly off the coast of Lobitos, Cabo Blanco, El Ñuro, Los Órganos, Cancas, and Punta Mero. After preliminary analysis, the available fisheries-dependent data were deemed too inconsistent or unreliable to contrast with the results of this study (e.g., landings recorded for Broomtail Grouper were zero in many years, whereas this species is consumed in restaurants across the country on a daily basis). In this case, future LEK-based assessments focused on bottom trolling and handline fishers would help to further understand the status of the Broomtail Grouper population.
Management implicationsMany of the species that were the focus of this study are only present in Peru, part of Chile, and a few sites within the Galapagos Islands. Some information on their status has been produced in Chile using diverse historical sources of information and mixed methods that include fisheries-dependent data, raising warnings about existing signs of overfishing for the Galapagos Sheephead Wrasse, Chino, and Negrillo (Godoy et al. 2010, 2016; Godoy Salinas 2013) and a critical need for management action with regard to the Chino, Negrillo, Galapagos Sheephead Wrasse, Pacific Beakfish, and Grape-eye Seabass (Araya et al. 2018; The Nature Conservancy 2018). Management agencies in Peru, Chile, and Ecuador would benefit from considering the results of studies based on historical sources of information, such as LEK, as a warning if overfishing and collapse of data-poor fisheries are to be prevented or reversed.
The results of this study provide evidence of the urgent need to start discussions on evaluating the precautionary implementation of fishing regulatory measures. We strongly suggest strict regulations, such as fishing closures, with the goal of recovering the populations and/or original distributions of species that are showing signs of overfishing and sequential depletion (Galapagos Sheephead Wrasse, Chino, Grape-eye Seabass, Harlequin Wrasse, and Pacific Goliath Grouper; Table 1). However, some of the selected species in our study, such as the Broomtail Grouper, have not been as severely impacted as those above. Management measures for these species may be less strict compared to a total fishery closure and instead could be based on spawning closures and/or the protection of essential habitat in response to reproductive behavior characterized by dense spawning aggregations that are susceptible to overharvest (Johannes 1997; Beets and Friedlander 1999; Johannes et al. 1999; Sala et al. 2001; Rhodes and Sadovy 2002; Aguilar-Perera 2006; Sadovy et al. 2008; Hughes et al. 2020). Based on the known reproductive biology and behavior of other Mycteroperca species, management of Broomtail Grouper could also be focused on size limits considering, for example, that they are most likely sequential hermaphrodites, with a portion of the older and larger fish transitioning from one sex to the other (McErlean and Smith 1964; Brulé et al. 2003). We recommend the widespread implementation of these measures across commercial and recreational fisheries in Peru.
ConclusionsIn this study, we elicited the LEK of 40 recreational and commercial spearfishers with between 5 and 30 years of experience. The elicitation methodology that was used enabled the systematization of experience and knowledge in a structured manner through the application of a clear and simple framework and the constant reinforcement of the objectives and limits of the questions as well as the quantitative boundaries expected from the answers (Tversky and Kahneman 1974; Burgman 2016; Hemming et al. 2018). Results suggest that the majority of the assessed species have experienced overfishing and geographically sequential exploitation based on indicators of the regular day-to-day catch in a series of fishing grounds and decades. Our study signals an urgent need to initiate management actions and adds to the growing literature supporting the use of historical sources of information in fisheries assessment.
ACKNOWLEDGMENTSThis study was funded by the Walton Family Foundation and Grant/Award Numbers ANID/PIA BASAL FB0002, ANID/Iniciativa Milenio/ICN 2019_015, and Proyecto ANID/BASAL FB210006. We greatly appreciate Luciano Pastorelli, Giulia Curatola, Francisco Meléndez, Simón Chapillequén, Ángel Calderón, Solange Alemán, Tullio Chapillequén, Javier Mogollón, Rosendo Mimbela, Juan Carlos Mústiga, Alfio Susti, Sergio Gonzáles, Alfonso Chávez, Rodrigo Suazo, Andrés Perona, Juani Pastorelli, Martín Salazar, Manuel Milla, Ana María Gallia Paredes, Martina Vazquez Soria, and all the spearfishers who kindly agreed to be interviewed in the study.
CONFLICT OF INTEREST STATEMENTThe authors report not to have any conflict of interest with respect to this study.
DATA AVAILABILITY STATEMENTOriginal data were obtained to perform the analyses included in this study and they can be accessed by directly writing to the corresponding author, who will gladly share them. Landings data from IMARPE (Instituto del Mar del Perú) are public and can be requested directly to that institution using the public information request platform.
ETHICS STATEMENTThe present study was developed following the Ethical Guidelines for Publication of Fisheries Research (Kočovský et al. 2019). No living being was directly observed, captured, retained, manipulated, transported, killed, analyzed, or disposed of during the development of this study. All the divers surveyed in this study gave their informed consent to be interviewed, after being provided with all relevant information about the purposes and methods of the study.
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Abstract
Objective
Fish populations targeted by recreational and artisanal fisheries remain largely unassessed in low- and middle-income countries. This generally results in a lack of regulatory action from government agencies, thus aggravating the risk of overfishing. In this context, sources of historical information, such as local ecological knowledge (LEK), are key to providing insight on the status of fish populations and informing management. Systematized elicitation processes have increasingly shown an ability to produce quantitative indicators while reducing biases and caveats inherent to expert knowledge. In this study, we assessed changes in composition of the catch, species abundance, and geographical distribution of the catch for 10 data-poor coastal groundfish species of Peru using LEK.
Methods
We designed and conducted a structured elicitation process to gather LEK on these species from 40 recreational and commercial spearfishers in Peru. We then used the obtained data to develop a set of indices and analyzed them statistically to identify trends and the magnitude of changes over time, if any, between the years 1960 and 2019.
Result
Our results show a significant decline in the relative participation (a species' catch proportion relative to the total catch) and abundance of seven assessed species in the catch as well as a major reduction in their geographical distribution. For some species, decreases in relative participation within the catch and decreases in average daily catch, a measure that may indicate changes in abundance, were statistically significant across the time span of the study. Average daily catch was between 1% and 15% of their historical high values. Some species have experienced a reduction of 60–100% in the geographical distribution of their catch.
Conclusion
Results suggests a scenario of overfishing and sequential depletion of the Galapagos Sheephead Wrasse
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Details
1 Sociedad Peruana de Derecho Ambiental, Lima, Peru
2 Centro de Investigación e Innovación para el Cambio Climático, Facultad de Ciencias, Universidad Santo Tomás, Santiago, Chile; Instituto Milenio en Socio-Ecología Costera and Institute of Ecology and Biodiversity, Santiago, Chile
3 The Nature Conservancy, Lima, Peru
4 Smithsonian's National Zoo and Conservation Biology Institute, Washington, D.C., USA; Asociación Peruana para la Conservación de la Naturaleza, Lima, Peru
5 Instituto Milenio en Socio-ecología Costera, Santiago, Chile; Center of Applied Ecology and Sustainability, Pontificia Universidad Católica de Chile, Santiago, Chile