Jennifer L. Waldo1,2,3*†
Ernesto Altamirano-Nieto4
Donald A. Croll2
Marta D. Palacios3,5,6†
Nerea Lezama-Ochoa3,7,8†
Jon Lopez4
Gala Moreno9
Stefany Rojas-Perea6Melissa R. Cronin2,3,10†- 1Department of Fisheries, Wildlife, and Conservation Sciences, Oregon State University, Corvallis, OR, United States
- 2Long Marine Lab, University of California Santa Cruz, Santa Cruz, CA, United States
- 3Mobula Conservation, La Paz, BCS, Mexico
- 4Inter-American Tropical Tuna Commission, La Jolla, CA, United States
- 5Instituto Politécnico Nacional, Centro Interdisciplinario de Ciencias Marinas, La Paz, Mexico
- 6The Manta Trust, Corscombe, Dorset, United Kingdom
- 7Institute of Marine Sciences, University of California Santa Cruz, Santa Cruz, CA, United States
- 8Ecosystem Science Division, National Oceanic and Atmospheric Administration (NOAA) Southwest Fisheries Science Center, Monterey, CA, United States
- 9International Seafood Sustainability Foundation, Washington, DC, United States
- 10Nicholas School of the Environment, Duke University, Durham, NC, United States
The incidental capture of non-target species (bycatch) in tuna fisheries impacts some marine vertebrates, particularly species with vulnerable life histories such as manta and devil rays (mobulids). There is broad interest in reducing mobulid bycatch in tuna purse seine fisheries, with existing efforts mainly focusing on reducing post-capture mortality rates. We explore a novel potential pre-capture mobulid bycatch avoidance strategy for the tuna purse seine fishery using communication between fishing vessels and associated spotter helicopters. We conducted a survey of tuna purse seine helicopter pilots, spotters, and fishers operating in the eastern Pacific Ocean (n = 33) to ascertain the ability of helicopter crew to detect mobulids prior to capture and communicate bycatch avoidance with vessel crew. Results indicate over half of the helicopter crew report being “always” or “sometimes” able to sight and identify mobulids and that helicopter crew regularly communicate mobulid sightings to the vessel already. Given that an average of 63% of class-6 vessel trips between 2017 to 2022 carried onboard helicopters, our results suggest that helicopter-vessel communication could be feasible and scalable for mobulid bycatch detection, enabling potential bycatch avoidance and early alerts for proper handling protocols. We also identify the potential use of helicopter detection to improve research efforts for mobulid conservation (e.g., data collection of population and habitat observations). This study is the first to investigate the utility of helicopter-vessel communication as a bycatch mitigation strategy for elasmobranchs and identifies research and management directions that could be further investigated to avoid bycatch of mobulids.
1 Introduction
The incidental capture of non-target species (bycatch) is one of the main drivers of population declines for several large marine vertebrate species (Myers and Worm, 2003; Lewison et al., 2004; Eddy et al., 2016). Sharks and rays (elasmobranchs), sea turtles, marine mammals, and seabirds are particularly at risk from bycatch due to vulnerable life history traits including slow growth, delayed maturity, and low fecundity (Gilman, 2011; Duffy et al., 2019).
Manta and devil rays (together referred to as mobulids) are filter-feeding species distributed globally in tropical and subtropical waters (Couturier et al., 2012; Stewart et al., 2018). Mobulids’ geographic ranges overlap with commercial tuna fisheries across multiple gears, creating the potential for incidental bycatch (Croll et al., 2012; Croll et al., 2016; Lezama-Ochoa et al., 2019b). Additionally, declines in mobulid populations have been observed globally (Couturier et al., 2012; Ward-Paige et al., 2013; Lezama-Ochoa et al., 2019b; Fernando and Stewart, 2021). As a result, all nine mobulid species are considered Vulnerable or Endangered on the International Union for Conservation of Nature Red List (IUCN, 2023). All mobulid species were also added to Appendices I and II of the Convention of Migratory Species (2015), which indicates conservation obligations for the protection of migratory species (Lezama-Ochoa et al., 2019b; Griffiths and Lezama-Ochoa, 2021) and to Appendix II of the Convention on International Trade in Endangered Species, which restricts international trade of listed species (Lyster, 1989; CITES, 2016). Despite these efforts, mobulid vulnerability to fisheries impacts persists (Croll et al., 2016; Fernando and Stewart, 2021; Griffiths and Lezama-Ochoa, 2021).
Some of the highest reports of mobulid catch and bycatch occur in the eastern Pacific Ocean (EPO), an important habitat for mobulids due to its favorable environmental conditions including seasonal upwelling and high productivity (Croll et al., 2016; Alfaro-Cordova et al., 2017; Lezama-Ochoa et al., 2019a). A total of 58,609 mobulids were caught by tuna fisheries operating in the EPO between 1993 and 2014, including all five species found in the EPO: oceanic manta ray (Mobula birostris), spinetail devil ray (M. mobular), sicklefin devil ray (M. tarapacana), bentfin devil ray (M. thurstoni), and pygmy devil ray (M. munkiana) (Lezama-Ochoa et al., 2019a). Further, captures of large mobulid aggregations have been recorded in this region, with reports of up to 220 individuals being caught in a single purse seine net (Lezama-Ochoa et al., 2019b; Palacios et al., 2023). EPO tuna purse seiners use three types of fishing strategies: nets deployed around schools of tuna associated with dolphins (dolphin sets), nets deployed around free-swimming schools of tuna (unassociated sets or school sets), and nets deployed around tunas aggregating near floating objects (natural log objects or fishing aggregating devices (FADs)) (Duffy et al., 2019; Lezama-Ochoa et al., 2019a). While tuna fishing sets and catches in the EPO increased from 2010-2019 and have generally remained steady in the EPO in recent years (IATTC, 2022), capture rates of the most frequently caught mobulid species (M. mobular) have decreased, suggesting populations in the region may be experiencing declines (White et al., 2015) given the species’ substantial increase in vulnerability status despite fishery closure periods in recent years (Griffiths and Lezama-Ochoa, 2021). In response, efforts to develop conservation and management measures have increased, including the employment and evaluation of best handling and release practices (Hutchinson et al., 2017; Hutchinson et al., 2023).
Several tuna Regional Fisheries Management Organizations (tRFMOs) have implemented conservation and management measures for mobulids across oceans (Duffy et al., 2019; Griffiths and Lezama-Ochoa, 2021). In 2015, the Inter-American Tropical Tuna Commission (IATTC), which manages tuna fisheries operating in the EPO, adopted Resolution C-15-04 which prohibits the “retention, transshipment, landing, storing, sale, or offering for sale of any part or whole carcass of mobulid rays by any commercial vessel” to encourage more sustainable tuna fishing operations (IATTC, 2015). The resolution also prohibits specific mobulid ray handling and manipulation methods (e.g., use of gaffs, hooks, or damage to the body or gills) and encourages proper handling and release methods for smaller individuals and new release handling techniques recommended by Poisson et al. (2014) (e.g., the use of a waste chute from the lower deck). Implementing appropriate best handling and release practices can reduce post-capture mortality rates by as little as 20%, as simulated for EPO tuna fisheries in 2018 (IATTC, 2023a).
Even with these fishery modifications, mobulids likely remain vulnerable to post-capture bycatch mortality (Stewart et al., 2018). Mobulids are obligate ram ventilators and require constant movement of water over their gills to breathe (Carlson et al., 2004). Further, mobulids lack a rigid skeleton to protect their internal organs, putting them at risk of internal injuries and crushing during handling (Poisson et al., 2014; Stewart et al., 2018). These traits emphasize the importance of developing effective bycatch avoidance or early release strategies to prevent or reduce mortality pre-capture, in addition to recent post-capture handling and releasing modifications.
The behavior and distribution of mobulids make developing pre-capture avoidance strategies challenging. First, mobulids share habitats with fishery target species (skipjack, yellowfin, and bigeye tuna), with co-occurrence mainly observed in free-swimming tuna school sets and dolphin-associated fishing sets (Lezama-Ochoa et al., 2019b). Second, some mobulid species (e.g., M. birostris and M. mobular) are highly migratory, traveling between productive regions to access oceanographic features with ephemeral prey availability, exposing them to bycatch across a broad geographic range; other species (e.g., M. munkiana) aggregate in specific coastal areas during different seasons for feeding or mating, exposing them to bycatch during vulnerable life history stages (Couturier et al., 2012; Croll et al., 2012; Lezama-Ochoa et al., 2019b; Andrzeiaczek et al., 2021; Palacios et al., 2021, 2023). Due to these broad distributions, inter-specific differences in movement patterns, and aggregative behaviour, it has been difficult to implement effective early avoidance and mitigation methods for all species.
Many bycatch mitigation programs have identified stakeholder collaboration and cooperation as key components to their success, as the application of bycatch mitigation measures is both a sociopolitical and an ecological endeavor (Moreno et al., 2007; Lewison et al., 2015; Hazen et al., 2018). Fishers have first-hand experience with vessel operations and bycatch protocols and are uniquely positioned to identify feasible mitigation methods (Matsushita et al., 2002; Cronin et al., 2023). The inclusion of fishers and fishery stakeholders in the development of novel bycatch mitigation can guide the implementation of more effective and adaptive bycatch mitigation (Hind, 2015; Stephenson et al., 2016; Watson et al., 2018; Cronin et al., 2023; Pol and Maravelias, 2023).
One way the involvement of fishers has helped address bycatch in dynamic environments is through the implementation of fleet-wide communication programs (Bethoney et al., 2017). Fleet communication programs prompt fishers of several vessels to act together sharing fishery information in real-time (Gilman et al., 2006; O’Keefe et al., 2014). Although fleet communication programs can be effective at reducing bycatch (Gilman et al., 2006), they often add additional costs and require voluntary uptake and communication from most vessels in a fleet (O’Keefe et al., 2014). Considering both these programs’ success and potential costs, a similarly modeled but smaller-scale approach to bycatch communication in the EPO using existing technology may be the first step to exploring the potential of communication programs.
Many large vessels in the EPO use spotter helicopters that fly miles ahead of the vessel in search of schools of fish and/or dolphins that tuna may be associated with (Lennert-Cody et al., 2016). Helicopters are usually single-rotor two-seater designs, operated by special crew members and include cockpits that allow a spotter to search for dolphins and tuna (Lennert-Cody et al., 2016; Trygg Mat Tracking and IMCS Network, 2021). Data from class-6 tuna purse seine vessels (i.e., vessels larger than 362 tons of carrying capacity) indicate that 69% of trips in 2022 carried an onboard helicopter (IATTC, unpublished data). In detail, aerial assistance was used for 99.7% of dolphin sets, 75.4% of unassociated sets, and 35.7% of floating object sets. Class-6 vessels account for roughly 75% of the purse seine fleet in the IATTC Convention Area and produce nearly 90% of the catch, demonstrating the potential for the use of helicopter-generated information to mitigate mobulid bycatch.
The ability of helicopter crew to sight dolphin pods and tuna from the air suggests they may also be able to sight other non-target near-surface swimming species in the area. Previous research on elasmobranchs conducted through aerial surveys at altitudes ranging 150m – 579m provide evidence that they are visible by plane when at the water’s surface (Figure 1; Notarbartolo-di-Sciara and Hillyer, 1989; Mullican et al., 2013; Kajiura and Tellman, 2016; Nykänen et al., 2018; Trujillo-Córdova et al., 2020). In a previous survey of tuna fishers from the EPO, a small number of helicopter pilot respondents reported being “sometimes” aware of mobulid presence before deploying the purse seine net in the water (Cronin et al., 2023). Mobulids may be recognizable from air because of their distinctive shape, large body size, prominent cephalic fins, dark coloration, tendency to swim and jump at the ocean’s surface, and tendency to aggregate in large schools (Notarbartolo-di-Sciara and Hillyer, 1989; Croll et al., 2012; Notarbartolo-di-Sciara et al., 2015; Francis and Jones, 2017; Palacios et al., 2023; S. Velazquez Hernandez, pers. comm., 22 December 2021). Communication between tuna helicopter pilots and their associated vessels about where mobulids are located could inform potential bycatch avoidance strategies in tuna purse seiners. This study investigates 1) the ability of tuna purse seine fishery helicopter crew to identify mobulids before the net is set, and 2) the potential feasibility of implementing bycatch communication protocols between helicopter and vessel crew. Given previous conservation gains from fleet communication programs, we hypothesize that within-vessel communication could be similarly feasible, particularly with vessels in a high-capacity fishery using spotting helicopters to facilitate fish-finding.
Figure 1 Aerial photos taken from a research seaplane of the following five Mobulid species found in the EPO: (A) M. birostris, (B) M. mobular, (C) M. tarapacana, (D) M. thurstoni, (E) M. munkiana. Photo credits: © Siddharta Velázquez Hernández, Ocean Life Flights.
2 Methods
We conducted structured surveys with helicopter pilots, spotters, and fishers with experience working in the EPO tropical tuna purse-seine fishery to understand 1) visual awareness of mobulids while on the helicopter, 2) differences between visual awareness of helicopter and vessel crew, and 3) existing habits of communicating with vessel crew and potential improvements to communicating mobulid presence.
2.1 Survey design and distribution
Surveys were administered in Spanish and English via the survey platform Qualtrics from February to July 2022 (UCSC IRB #HS-FY2022-156). Survey results were translated into English using a translation service before analysis. All respondents read and agreed to a consent form before participating which instructed that all survey questions were voluntary and confidential. Survey questions were grouped into four categories: 1) experience as helicopter crew, 2) indicators used to sight species, 3) visual identification of species, and 4) communication with the vessel (Table 1).
Table 1 Survey questions included in this study.
2.2 Data analysis
Participants were split into two groups based on whether they had experience as a pilot or spotter on a tuna vessel helicopter (“helicopter crew”) or not (“vessel crew”). Survey results were sorted and analyzed using the dplyr package in R version 4.0.4 (Wickham et al., 2023). Responses to multiple-choice questions about participants’ ability to sight bycatch species were placed on a four-point scale and analyzed using the likert package in R (Bryer and Speershneider, 2016). To understand mobulids’ likelihood of being sighted relative to other large vertebrates, these questions were asked separately for four species groups commonly bycaught in the EPO: mobulids, dolphins, sea turtles, and sharks. The IATTC has specific requirements for purse seine vessels to release these species of interest (IATTC, 2006; IATTC, 2011; IATTC, 2019; IATTC, 2023b), therefore the crew needs to be aware of the species’ presence to comply with the commission’s requirements.
Each analysis was conducted using a two-tailed test and P-values below 0.05 were considered significant. We performed a Shapiro test for normality using the stats package in base R (R Core Team, 2023), which indicated data did not follow a normal distribution. Kruskal-Wallis tests were used to test for differences between independent responses. For data comparing more than two independent variables, such as between responses comparing the four bycatch species groups, post hoc Wilcoxon signed-rank tests were used to test for differences between paired answers. Effect sizes were calculated to measure the strength of the relationship (Kruskal-Wallis test: small effect = 0.01–0.06, moderate effect = 0.06–0.14, large effect = >0.14; Wilcoxon signed-rank test: small effect = 0.10–0.30, moderate effect = 0.30–0.50, large effect = >0.50). Participants who did not respond to a given question were excluded from the analysis of that question, therefore questions differ in their number of respondents.
3 Results
A total of 33 tuna purse seine fishers operating in the EPO were surveyed. 30% of the respondents (n = 10) had experience as helicopter crew, while 70% (n = 23) of respondents did not. The survey sample size was limited and constrained by the number of eligible accessible participants, particularly for helicopter crew.
3.1 Visual identification of species
When asked about their ability to sight and identify mobulids, helicopter crew were more likely to report “always” or “sometimes” being able to identify the species of mobulid than vessel crew (Kruskal-Wallis test: p < 0.05; effect size = moderate; Figure 2A), and were more likely to “always” or “sometimes” be able to sight an individual mobulid compared to vessel crew (Kruskal-Wallis test: p < 0.01; effect size = large; Figure 2C). Respondents’ ability to “always” or “sometimes” sight mobulid schools was higher for helicopter crew (40%; n = 4) than vessel crew (10%; n = 2; Figure 2B) and overall, 85% of respondents (n = 23) said less than 10 individuals are needed to sight a mobulid school.
Figure 2 Fishers’ ability to identify the species of mobulid, sight schools of mobulids, sight individual mobulids, and frequency of communicating mobulid sightings. Grouped by experience as tuna purse seine helicopter crew (n = 10) or no experience as helicopter crew (n = 20). * = p < .05 ** = p < .01.
Comparing the four taxonomic groups, more respondents reported being “always” or “sometimes” able to sight a dolphin school than a mobulid school (Kruskal-Wallis test: p < 0.001; Wilcoxon signed-rank test: p < 0.001; effect size = large; Supplementary Figures S1, S2). Respondents were also more likely to “always” or “sometimes” be able to identify the species of dolphin compared to the species of mobulid (Wilcoxon signed-rank test: p < 0.05; effect size = moderate; Supplementary Figure S2). When asked what the easiest marine animals are to sight, mobulids were the third most frequently reported species (18%; n = 6), following dolphins (76%; n = 25) and whales (55%; n = 18).
3.2 Communication with the vessel
All helicopter crew respondents said they “always” or “sometimes” communicate mobulid sightings. This was significantly more frequent than vessel crew, of whom 60% reported “always” or “sometimes” communicating mobulid sightings (Kruskal-Wallis test: p < 0.05; effect size = moderate; Figure 2D). In comparison, all but one respondent said they “always” or “sometimes” communicate dolphin sightings to the vessel (Supplementary Figure S1).
For the type of information communicated regarding species sightings, respondents said they routinely communicate the type of tuna (97%; n = 28), the location of tuna (79%; n = 25), and the number of tuna (69%; n = 20; Figure 3A). More than half of respondents said they communicate the type of bycatch species (66%; n = 19), followed by the location of that species (52%; n = 15) and the number of individuals of that species (45%; n = 13; Figure 3A). Vessel crew were slightly more likely to report specific information about bycatch species sightings while helicopter crew were slightly more likely to report specific information about tuna sightings (Figure 3B).
Figure 3 (A) Information EPO tuna purse seine fishers routinely communicate to vessel crew (N = 29). (B) Responses separated by the proportions of helicopter crew (N = 10; in red) and the proportions of vessel crew (N = 19; in blue). Data are expressed as the proportion ± margin of error.
When asked how much additional time it would take to communicate information about bycatch species presence, 60% of helicopter crew respondents (n = 6) said it would add less than five minutes to routine communication, 30% (n = 3) said five to ten minutes, and 10% (n = 1) said ten to fifteen minutes.
Participants made several recommendations for improving within-vessel communication about bycatch. Respondents suggested implementing: 1) more detailed coordination between the helicopter and the vessel (e.g., reporting the specific species and its location), and 2) improving maneuvering (e.g., separating bycatch and target species before setting or removing bycatch from the net).
3.3 Indicators used to sight species
For the indicators used to sight bycatch species, most fishers reported using the color of the species as an indicator of its presence (47%; n = 14), but others included the species’ behavior, shape, jumps, fins, size, schooling behavior, and the presence of birds. For mobulids specifically, their behavior to jump was the highest given response (56%; n = 15), followed by their color (11%; n = 3), shape (11%; n = 3), movements (7%; n = 2), number of individuals (4%; n = 1), and the presence of birds (4%; n = 1).
In addition, respondents were asked what environmental conditions affect their ability to sight bycatch species. Weather (48%; n = 15) was the most reported answer, followed by sea state (i.e., wind, waves, and swell of the ocean’s surface) (35%; n = 11), time of day (23%; n = 7), and light conditions (19%; n = 6). These factors can prevent the visibility of species in the water, as one respondent wrote that light conditions and weather are especially obstructive when the weather is cloudy, and the color of the species is not visible.
4 Discussion
This is the first study to investigate communication between helicopter and vessel crew about mobulid sightings as a potential pre-capture avoidance strategy for mobulid bycatch. There are limitations associated with the small sample size of this study due to a limited number of vessels currently using helicopters and limited access to this specific crew – generally, only class-6 vessels carry helicopters, and aerial assistance on these vessels may come from either their onboard helicopter, the helicopter of another vessel, or a spotter plane. Nevertheless, our analysis suggests helicopter crew may be more successful in sighting mobulids and are more likely to communicate information about mobulid sightings, creating new opportunities to reduce mobulid bycatch. These results provide guidance on factors influencing mobulid sightings and information that is currently routinely communicated, which could aid in developing protocols for reporting mobulid presence to the vessel.
Participants with helicopter experience were more likely to report an ability to sight an individual mobulid and identify the species of mobulid compared to other vessel crew, suggesting that helicopter crew may be more useful in locating mobulid presence. It should be noted that participants may have interpreted the species identification question as referencing the identification of mobulid rays, rather than the specific species of mobulid. Even so, these results are consistent with a previous study investigating mobulid bycatch mitigation methods in New Zealand, in which two interviewed spotter plane pilots said that mobulids were visible from the air and they felt capable of distinguishing between different mobulid species (Jones and Francis, 2012). Previous studies using spotter planes to identify aggregation sites of M. mobular in the Mediterranean and M. birostris in the Caribbean Seas additionally demonstrate the ability to spot and differentiate between mobulids from the air (Notarbartolo-di-Sciara and Hillyer, 1989; Duffy and Abbott, 2003; Notarbartolo-di-Sciara et al., 2015). Pilots aboard these spotter planes were likely well-trained to identify mobulids but highlight the potential for training helicopter crew on species identification to differentiate between mobulid species.
Dolphins were the easiest species to sight and dolphin schools were more likely to be sighted compared to mobulid schools. These results are unsurprising, given the size of the aggregation of dolphin schools. In fact, dolphin schools are used as an indicator of tuna presence in the EPO (Polacheck, 1989; Lewison et al., 2004; Lennert-Cody et al., 2016; Ward et al., 2018). If fishers are already looking for dolphin schools and already know what indicators to look for to do so, it is conceivable that dolphins could be a model and the use of similar visual indicators could be explored as a way of improving the sighting of mobulids and other bycatch species of similar size and characteristics.
Given the ability of helicopter crew to see mobulids while searching for tuna and the reported ease of communicating this information, helicopter-vessel communication could be a feasible bycatch mitigation strategy for mobulids, on the condition that communication and coordination between helicopter and vessel crew are improved by including more information on the presence of bycatch species that can be factored into purse seine sets. This communication should include in-depth information about the species, number, and location of mobulid presence. Information could be shared within vessels and between vessels, particularly for vessels cooperatively fishing in groups (Lennert-Cody et al., 2020). Communication could also include whether mobulids are observed alone or in large schools. Though mobulids are more frequently caught in low numbers per set (Lezama-Ochoa et al., 2019b), all mobulid species are documented to undergo aggregation behavior (Palacios et al., 2023) and large aggregations (more than 50 individuals) of some species in the EPO have been observed and captured by sets (Lezama-Ochoa et al., 2019b). To scale the helicopter information and to provide alternative solutions for vessels that do not carry a helicopter, there may be potential to establish a comprehensive onshore open reporting system – like a fleet-wide communication program. If supported by the Regional Fisheries Management Organizations, the system could collect and report real-time information to all registered fleets operating in the area. One example of where a similar helicopter reporting system has been applied in the conservation context is in the heli-ski industry, whereby one company has their guides report caribou sightings via a proprietary tool; the tool alerts other guides in the company when there’s a high chance of seeing a caribou in a specific area for them to avoid (Williamson, 2024).
In addition to improved communication, we suggest that improving the helicopter crew’s ability to sight bycatch species while searching for tuna may aid in advancing their communication and applying this bycatch avoidance strategy to other vulnerable species, such as sea turtles and sharks. The ability of purse seine fishery crew and observers to accurately identify the mobulid species is low (Lezama-Ochoa et al., 2019b). Training helicopter crew on species identification could additionally help improve their ability to sight mobulids and possibly differentiate between species when reporting sightings to the vessel. Helicopter crew could be provided with a species identification guidebook that includes aerial images of various bycatch species and the indicators they can use to sight them. Similar guidebooks are often distributed to fishery observers and crew in industrial tuna fisheries (Chapman and Secretariat of the Pacific Community, 2006; Fukofuka and Itano, 2006; Stevens, 2011; Park, 2019), and could be adapted for aerial perspective. Significant efforts are currently being conducted to improve species identification in the EPO, such as the development of smart tools based on artificial intelligence or genetic information, or simpler approaches like the development of mobulid species identification guides for observers and fishers (e.g., IATTC SAC-13-01). Educational posters on mobulid identification have also been distributed for tuna fishers in each ocean (Cronin et al., 2023), which could be adapted for use in an aerial setting. Crew’s identification skills could also be improved through training workshops. Skipper workshops have previously been conducted to teach crew about advances in bycatch mitigation methods and regulation (Murua et al., 2019; Murua et al., 2023). Adding scientist-led training on species identification during these workshops could improve the crew’s ability to identify non-target species; similar workshops can be implemented specifically with the helicopter crew for species identification from an aerial view.
Although almost all effect sizes for significant results were large, the small sample size of this study (n = 33) is a limitation — however, we suggest these results as an indicator of directions for future research. Short-term research directions include: investigating potential incentives for the fleet to improve communication, incentives for bycatch avoidance if helicopter-vessel communication is further considered as an option, and measuring the vessel response time to helicopter-vessel communication. Additionally, we recommend exploring the development of feasible modifications of the net setting process that can effectively translate non-target species information communicated from the helicopter into reduced bycatch in net sets. For instance, several respondents made suggestions of using helicopter information as an alert to maneuver according to the non-target species’ location before setting the net. RFMOs should concentrate their efforts on bycatch avoidance strategies, such as this one, considering the vulnerability status of mobulids and other commonly caught species. However, when isolating the species is not possible, information could serve as an early alert for the species’ quick release knowing it will be in the set. Finally, as this sample only encompasses vessels with onboard helicopters operating in the EPO, future research should explore similar methods for identifying mobulid presence and taking preventive measures, including avoiding their capture, that could apply to vessels without helicopters, including dynamic management applications based on remote sensing, drones, sonar, and other emerging technologies (Howell et al., 2008; Moreno et al., 2016; Hazen et al., 2018; Cronin et al., 2023). For vessels without helicopters, the crow’s nest serves as an observation platform equipped with high-resolution binoculars and viewing ranges of up to 19 miles in good conditions (Green et al., 1971). This view enables fishers to spot tuna – and potentially detect non-target species – much like they do from helicopters, caveating for the reduced visibility of species at depth.
This study highlights the valuable information that helicopter pilots could provide to scientists on the presence of mobulids and other species in specific areas. Increasing knowledge of mobulid populations and their habitats is a research priority (Stewart et al., 2018; Lezama-Ochoa et al., 2019b; Palacios et al., 2023), but investigating these species in the open ocean is often difficult and costly. Helicopter crew might see mobulids during flights but not report these sightings because there is currently no protocol or requirement to do so, other than cases for which fishing operations commence and observers must record any caught mobulids. The use of helicopter crew as observers of the pelagic environment could help fill important knowledge gaps about the spatial and temporal distribution of mobulids and other pelagic species and should be further considered in the EPO.
Bycatch avoidance programs have been most effective when integrated with existing or impending regulations (Bethoney et al., 2017). Despite the small sample size of this study, it could be suggested that combining pre-capture avoidance strategies, such as helicopter-vessel communication, with improved post-capture handling and release methods collectively could significantly mitigate mobulid bycatch and mortality in tuna purse seine fisheries. Helicopter-vessel communication could not only assist avoiding capture but also be an early alert system to the vessel that a mobulid is likely to be in the fishing gear, allowing the vessel crew to prepare for best handling practices for a more efficient release. This study explores a novel application of existing technology for mobulid bycatch avoidance to innovatively include fishers’ knowledge and help meet fisheries management goals.
Data availability statement
The data underlying this article cannot be shared publicly to protect the privacy of individuals who participated in the study. The data will be shared on reasonable request to the corresponding author.
Ethics statement
The studies involving humans were approved by University of California Santa Cruz Office of Research Compliance Administration. The studies were conducted in accordance with the local legislation and institutional requirements. The participants provided their written informed consent to participate in this study.
Author contributions
JW: Conceptualization, Data curation, Formal analysis, Funding acquisition, Investigation, Methodology, Project administration, Resources, Software, Validation, Visualization, Writing – original draft, Writing – review & editing. EA: Data curation, Resources, Writing – review & editing. DC: Supervision, Writing – review & editing. MP: Methodology, Resources, Writing – review & editing. NL: Methodology, Writing – review & editing. JL: Data curation, Resources, Writing – review & editing. GM: Data curation, Methodology, Writing – review & editing. SR: Writing – review & editing. MC: Conceptualization, Data curation, Methodology, Resources, Supervision, Writing – review & editing, Funding acquisition, Investigation, Software.
Funding
The author(s) declare that financial support was received for the research, authorship, and/or publication of this article. Publication of this paper was supported by the Thomas G. Scott Publication Funds and the Western Division of the American Fisheries Society Small Project Grant. This research was additionally supported by the Undergraduate Research in Science & Technology Endowment and the Stevenson College Student Research Project Award from the University of California, Santa Cruz.
Acknowledgments
The authors would like to acknowledge the Inter-American Tropical Tuna Commission, TUNACONS, and the International Seafood Sustainability Foundation for helping to collect the data for this study. The authors are thankful to Mobula Conservation for facilitating this research and Kelly Zilliacus for logistical support. We also thank Siddharta Velázquez and Leonardo Silva for providing extensive background information through informal interviews. Finally, the authors are grateful to the fishers who participated in this study, as this research would not be possible without their valuable knowledge.
Conflict of interest
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
Publisher’s note
All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher.
Supplementary material
The Supplementary Material for this article can be found online at: https://www.frontiersin.org/articles/10.3389/fmars.2024.1303324/full#supplementary-material
References
Alfaro-Cordova E., Del Solar A., Alfaro-Shigueto J., Mangel J. C., Diaz B., Carrillo O., et al. (2017). Captures of manta and devil rays by small-scale gillnet fisheries in northern Peru. Fish. Res. 195, 28–36. doi: 10.1016/j.fishres.2017.06.012
Andrzeiaczek S., Schallert R. J., Forsberg K., Arnoldi N. S., Cabanillas-Torpoco M., Purizaca W., et al. (2021). Reverse diel vertical movements of oceanic manta rays off the northern coast of Peru and implications for conservation. Ecol. Solutions Evid. 2, e12051. doi: 10.1002/2688-8319.12051
Bethoney N. D., Schondelmeier B. P., Kneebone J., Hoffman W. S. (2017). Bridges to best management: Effects of a voluntary bycatch avoidance program in a mid-water trawl fishery. Mar. Policy 83, 172–178. doi: 10.1016/j.marpol.2017.06.003
Bryer J., Speershneider K. (2016) likert: Analysis and Visualization Likert Items (1.3.5) [R]. Available online at: http://jason.bryer.org/likert.
Carlson J., Goldman K., Lowe C. (2004). “Metabolism, energetic demand, and endothermy,” in Biology of Sharks and Their Relatives, vol. 20043354 . Eds. Musick J., Carrier J., Heithaus &M. (Boca Raton, Florida, USA: CRC Press), 203–224. doi: 10.1201/9780203491317.ch7
Chapman L. B. and Secretariat of the Pacific Community. (2006). Marine species identification manual for horizontal longline fishermen (Noumea Cedex, New Caledonia: Secretariat of the Pacific Community).
CITES. (2016). Consideration of proposals for amendment of appendix I and II. (CoP17 prop. 44). Available online at: https://cites.org/sites/default/files/eng/cop/17/prop/060216/E-CoP17Prop-44.pdf.
Couturier L. I. E., Marshall A. D., Jaine F. R. A., Kashiwagi T., Pierce S. J., Townsend K. A., et al. (2012). Biology, ecology and conservation of the mobulidae. J. Fish. Biol. 80, 1075–1119. doi: 10.1111/j.1095-8649.2012.03264.x
Croll D., Newton K., Weng K., Galván-Magaña F., O’Sullivan J., Dewar H. (2012). Movement and habitat use by the spine-tail devil ray in the Eastern Pacific Ocean. Mar. Ecol. Prog. Ser. 465, 193–200. doi: 10.3354/meps09900
Croll D. A., Dewar H., Dulvy N. K., Fernando D., Francis M. P., Galván-Magaña F., et al. (2016). Vulnerabilities and fisheries impacts: The uncertain future of manta and devil rays. Aquat. Conservation: Mar. Freshw. Ecosyst. 26, 562–575. doi: 10.1002/aqc.2591
Cronin M. R., Croll D. A., Hall M. A., Lezama-Ochoa N., Lopez J., Murua H., et al. (2023). Harnessing stakeholder knowledge for the collaborative development of mobulid bycatch mitigation strategies in tuna fisheries.. ICES J. Mar. Sci. 80 (3), 620–634. doi: 10.1093/icesjms/fsac093
Duffy C. A. J., Abbott D. (2003). Sightings of mobulid rays from northern New Zealand, with confirmation of the occurrence of Manta birostris in new Zealand waters. NZ. J. Mar. Fresh. Res. 37, 715–721. doi: 10.1080/00288330.2003.9517201
Duffy L. M., Lennert-Cody C. E., Olson R. J., Minte-Vera C. V., Griffiths S. P. (2019). Assessing vulnerability of bycatch species in the tuna purse-seine fisheries of the eastern Pacific Ocean. Fish. Res. 219, 105316. doi: 10.1016/j.fishres.2019.105316
Eddy C., Brill R., Bernal D. (2016). Rates of at-vessel mortality and post-release survival of pelagic sharks captured with tuna purse seines around drifting fish aggregating devices (FADs) in the equatorial eastern Pacific Ocean. Fish. Res. 174, 109–117. doi: 10.1016/j.fishres.2015.09.008
Fernando D., Stewart J. D. (2021). High bycatch rates of manta and devil rays in the “small-scale” artisanal fisheries of Sri Lanka. PeerJ 9, e11994. doi: 10.7717/peerj.11994
Francis M. P., Jones E. G. (2017). Movement, depth distribution and survival of spinetail devilrays (Mobula Japanica) tagged and released from purse-seine catches in New Zealand: Movement, depth distribution and survival of spinetail devilrays. Aquat. Conservation: Mar. Freshw. Ecosyst. 27, 219–236. doi: 10.1002/aqc.2641
Fukofuka S., Itano D. G. (2006). A Handbook for the Identification of Yellowfin and Bigeye Tunas in Fresh, but Less Than Ideal Condition (v6). (Noumea, New Caledonia: Western and Central Pacific Fisheries Commission), Vol. 57.
Gilman E. L., Dalzell P., Martin S. (2006). Fleet communication to abate fisheries bycatch. Mar. Policy 30, 360–366. doi: 10.1016/j.marpol.2005.06.003
Gilman E. L. (2011). Bycatch governance and best practice mitigation technology in global tuna fisheries. Mar. Policy 35, 590–609. doi: 10.1016/j.marpol.2011.01.021
Green R. E., Pervin W. F., Petrich B. P. (1971). The American Tuna Purse Seine Fishery. (London, England: Fishing News (Books) Ltd), Vol. 3. 182–194.
Griffiths S. P., Lezama-Ochoa N. (2021). A 40-year chronology of the vulnerability of spinetail devil ray (Mobula mobular) to eastern Pacific tuna fisheries and options for future conservation and management. Aquat. Conservation: Mar. Freshw. Ecosyst. aqc.3667, 2910–2925. doi: 10.1002/aqc.3667
Hazen E. L., Scales K. L., Maxwell S. M., Briscoe D. K., Welch H., Bograd S. J., et al. (2018). A dynamic ocean management tool to reduce bycatch and support sustainable fisheries. Sci. Adv. 4, eaar3001. doi: 10.1126/sciadv.aar3001
Hind E. J. (2015). A review of the past, the present, and the future of fishers’ knowledge research: A challenge to established fisheries science. ICES J. Mar. Sci. 72, 341–358. doi: 10.1093/icesjms/fsu169
Howell E., Kobayashi D., Parker D., Balazs G., Polovina J. J. (2008). TurtleWatch: A tool to aid in the bycatch reduction of loggerhead turtles Caretta caretta in the Hawaii-based pelagic longline fishery. Endangered Species Res. 5, 267–278. doi: 10.3354/esr00096
Hutchinson M., Poisson F., Swimmer Y. (2017). Developing best handling practice guidelines to safely release mantas, mobulids and stingrays captured in commercial fisheries. Pacific Islands Fish. Sci. Center (U.S.). doi: 10.7289/V5/WP-PIFSC-17-006
Hutchinson M., Lopez J., Wiley B., Pulvenis J.-F., Altamirano E., Aires-da-Silva A. (2023). Knowledge and research gaps to the implementation of best handling and release practices for vulnerable species (Document EB-01-01; Working Group on Ecosystem & Bycatch) (La Jolla, California, USA: Inter-American Tropical Tuna Commission).
IATTC (2006). Consolidated resolution on bycatch (Resolution C-04-05 (Rev 2)) (Pusan, Korea: Inter-American Tropical Tuna Commission).
IATTC (2011). Resolution on the conservation of oceanic whitetip sharks caught in association with fisheries in the Antigua Convention Area (Resolution C-11-10) (La Jolla, California, USA: Inter-American Tropical Tuna Commission).
IATTC (2015). Resolution on the conservation of Mobulid rays caught in association with fisheries in the IATTC convention area (C-15–04) (Guayaquil, Ecuador: Inter-American Tropical Tuna Commission).
IATTC (2019). Resolution to mitigate impacts on sea turtles (Resolution C-19-04) (Bilbao, Spain: Inter-American Tropical Tuna Commission).
IATTC (2022). Report on the Tuna Fishery, Stocks, and Ecosystem in the Eastern Pacific Ocean in 2021 (IATTC-100-01) (Phoenix, Arizona, USA: Inter-American Tropical Tuna Commission).
IATTC (2023a). Conservation measures for shark species, with special emphasis on the silky shark (Carcharhinus falciformis), for the years 2024 and 2025 (Resolution C-23-08) (Victoria, B.C., Canada: Inter-American Tropical Tuna Commission).
IATTC (2023b). Ecosystem Considerations (SAC-14-11) (La Jolla, California, USA: Inter-American Tropical Tuna Commission).
IUCN (2023) The IUCN Red List of Threatened Species (No. 2022–2). Available online at: https://www.iucnredlist.org.
Jones E., Francis M. (2012). Protected rays – occurrence and development of mitigation methods in the New Zealand tuna purse seine fishery (Contract 4352). Department of Conservation 39.
Kajiura S. M., Tellman S. L. (2016). Quantification of massive seasonal aggregations of blacktip sharks (Carcharhinus limbatus) in Southeast Florida. PloS One 11, e0150911. doi: 10.1371/journal.pone.0150911
Lennert-Cody C. E., Maunder M. N., Fiedler P. C., Minami M., Gerrodette T., Rusin J., et al. (2016). Purse-seine vessels as platforms for monitoring the population status of dolphin species in the eastern tropical Pacific Ocean. Fish. Res. 178, 101–113. doi: 10.1016/j.fishres.2015.10.005
Lennert-Cody C. E., Maunder M. N., Román M. H., Xu H., Minami M., Lopez J. (2020). Cluster analysis methods applied to daily vessel location data to identify cooperative fishing among tuna purse-seiners. Environ. Ecol. Stat 27, 649–664. doi: 10.1007/s10651-020-00451-7
Lewison R., Crowder L., Read A., Freeman S. (2004). Understanding impacts of fisheries bycatch on marine megafauna. Trends Ecol. Evol. 19, 598–604. doi: 10.1016/j.tree.2004.09.004
Lewison R., Hobday A. J., Maxwell S., Hazen E., Hartog J. R., Dunn D. C., et al. (2015). Dynamic ocean management: identifying the critical ingredients of dynamic approaches to ocean resource management. BioScience 65, 486–498. doi: 10.1093/biosci/biv018
Lezama-Ochoa N., Hall M. A., Pennino M. G., Stewart J. D., López J., Murua H. (2019b). Environmental characteristics associated with the presence of the Spinetail devil ray (Mobula mobular) in the eastern tropical Pacific. PloS One 14, e0220854. doi: 10.1371/journal.pone.0220854
Lezama-Ochoa N., Hall M., Román M., Vogel N. (2019a). Spatial and temporal distribution of mobulid ray species in the eastern Pacific Ocean ascertained from observer data from the tropical tuna purse-seine fishery. Environ. Biol. Fishes 102, 1–17. doi: 10.1007/s10641-018-0832-1
Lyster S. (1989). The convention on the conservation of migratory species of wild animals (The bonn convention). Natural Resour. J. 29, 23.
Matsushita Y., Glass C. W., Morris G. D., Feehan T. L., Sarno B. (2002). Taking fishermen’s knowledge into conservation harvesting technology research and development a case study in New England, USA. Fish. Sci. 68, 376–379. doi: 10.2331/fishsci.68.sup1_376
Moreno G., Dagorn L., Capello M., Lopez J., Filmalter J., Forget F., et al. (2016). Fish aggregating devices (FADs) as scientific platforms. Fish. Res. 178, 122–129. doi: 10.1016/j.fishres.2015.09.021
Moreno G., Dagorn L., Sancho G., Itano D. (2007). Fish behaviour from fishers’ knowledge: The case study of tropical tuna around drifting fish aggregating devices (DFADs). Can. J. Fish. Aquat. Sci. 64, 1517–1528. doi: 10.1139/f07-113
Mullican T., Hampp J., Tyminksi J. (2013). Aerial survey & satellite tagging of Manta Rays in coastal waters of Northeast Florida. J. Mar. Sci.: Res. Dev. s1, 70. doi: 10.4172/2155-9910.S1.002
Murua J., Moreno G., Dagorn L., Itano D., Hall M., Murua H., et al. (2023). Improving sustainable practices in tuna purse seine fish aggregating device (FAD) fisheries worldwide through continued collaboration with fishers. Front. Mar. Sci. 10. doi: 10.3389/fmars.2023.1074340
Murua J., Moreno G., Itano D., Hall M., Dagorn L., Restrepo V. (2019). ISSF skippers’ workshops round 8. ISSF technical report 2019-01. Washington, D.C., USA: International Seafood Sustainability Foundation.
Myers R. A., Worm B. (2003). Rapid worldwide depletion of predatory fish communities. Nature 423, 280–283. doi: 10.1038/nature01610
Notarbartolo-di-Sciara G., Hillyer E. V. (1989). Mobulid Rays off Eastern Venezuela (Chondrichthyes, mobulidae). Copeia 1989, 607. doi: 10.2307/1445487
Notarbartolo-di-Sciara G., Lauriano G., Pierantonio N., Cañadas A., Donovan G., Panigada S. (2015). The devil we don’t know: investigating habitat and abundance of endangered giant devil rays in the north-Western Mediterranean Sea. PloS One 10, e0141189. doi: 10.1371/journal.pone.0141189
Nykänen M., Jessopp M., Doyle T. K., Harman L. A., Cañadas A., Breen P., et al. (2018). Using tagging data and aerial surveys to incorporate availability bias in the abundance estimation of blue sharks (Prionace glauca). PloS One 13, e0203122. doi: 10.1371/journal.pone.0203122
O’Keefe C. E., Cadrin S. X., Stokesbury K. D. E. (2014). Evaluating effectiveness of time/area closures, quotas/caps, and fleet communications to reduce fisheries bycatch. ICES J. Mar. Sci. 71, 1286–1297. doi: 10.1093/icesjms/fst063
Palacios M. D., Hoyos-Padilla E. M., Trejo-Ramírez A., Croll D. A., Galván-Magaña F., Zilliacus K. M., et al. (2021). Description of first nursery area for a pygmy devil ray species (Mobula munkiana) in the Gulf of California, Mexico. Sci. Rep. 11, 132. doi: 10.1038/s41598-020-80506-8
Palacios M. D., Stewart J. D., Croll D. A., Cronin M. R., Trejo-Ramírez A., Stevens G. M. W., et al. (2023). Manta and devil ray aggregations: Conservation challenges and developments in the field. Front. Mar. Sci. 10. doi: 10.3389/fmars.2023.1148234
Park T. (2019). Shark and ray identification manual for observers and crew of the western and central Pacific tuna fisheries (Noumea, New Caledonia: Pacific Community).
Poisson F., Séret B., Vernet A.-L., Goujon M., Dagorn L. (2014). Collaborative research: Development of a manual on elasmobranch handling and release best practices in tropical tuna purse-seine fisheries. Mar. Policy 44, 312–320. doi: 10.1016/j.marpol.2013.09.025
Pol M., Maravelias C. D. (2023). Cracking the challenges of incentivizing avoidance of unwanted catch. ICES J. Mar. Sci. 80, 403–406. doi: 10.1093/icesjms/fsad047
Polacheck T. (1989). Analysis of the relationship between the distribution of searching effort, tuna catches, and dolphin sightings within individual purse seine cruises. Fish. Bull. (Washington, D.C.) 86 (2), 16.
R Core Team (2023). R: A language and environment for statistical computing. [R] (Vienna, Austria: R Foundation for Statistical Computing). Available at: https://www.R-project.org/.
Stephenson R. L., Paul S., Pastoors M. A., Kraan M., Holm P., Wiber M., et al. (2016). Integrating fishers’ knowledge research in science and management. ICES J. Mar. Sci. 73, 1459–1465. doi: 10.1093/icesjms/fsw025
Stevens G. (2011). Field Guide to the Identification of mobulid Rays (mobulidae): Indo-West Pacific (Dorset, UK: Manta Trust).
Stewart J. D., Jaine F. R. A., Armstrong A. J., Armstrong A. O., Bennett M. B., Burgess K. B., et al. (2018). Research priorities to support effective manta and devil ray conservation. Front. Mar. Sci. 5. doi: 10.3389/fmars.2018.00314
Trujillo-Córdova J. A., Mimila-Herrera E., Cárdenas-Palomo N., Herrera-Silveira J. A. (2020). Use of aerial surveys for assessing abundance of the whale shark (Rhincodon typus) and the giant manta (Mobula birostris) in the northern Caribbean Sea off Mexico. Fish. Bull. 118, 240–249. doi: 10.7755/FB.118.3.3
Trygg Mat Tracking, IMCS Network (2021). A MCS Practitioners Introductory Guide to: Purse Seine Fishing. (Oslo, Norway; Trygg Mat Tracking and IMCS Network).
Ward T. M., Ivey A., Carroll J. (2018). Code of practice for reducing accidental mortality of dolphins in purse-seine fisheries. Mar. Policy 87, 203–211. doi: 10.1016/j.marpol.2017.10.032
Ward-Paige C. A., Davis B., Worm B. (2013). Global population trends and human use patterns of manta and mobula rays. PloS One 8, e74835–e74835. doi: 10.1371/journal.pone.0074835
Watson M. S., Cook K. V., Young N., Hinch S. G. (2018). Perceptions and actions of commercial fishers in response to conservation measures in Canadian Pacific salmon fisheries. Trans. Am. Fish. Soc. 147, 906–918. doi: 10.1002/tafs.10073
White E. R., Myers M. C., Flemming J. M., Baum J. K. (2015). Shifting elasmobranch community assemblage at Cocos Island—An isolated marine protected area. Conserv. Biol. 29, 1186–1197. doi: 10.1111/cobi.12478
Wickham H., François R., Müller K., Vaughan D. (2023) dplyr: A Grammar of Data Manipulation [R]. Available online at: https://dplyr.tidyverse.orghttps://github.com/tidyverse/dplyr.
Williamson A. C. (2024). When epic ski trips and caribou conservation collide (The Narwhal). Available at: https://thenarwhal.ca/bc-heli-skiing-caribou/. illustrations by Simone.
Keywords: purse seine, management, eastern Pacific Ocean, stakeholder knowledge, elasmobranch, conservation technology
Citation: Waldo JL, Altamirano-Nieto E, Croll DA, Palacios MD, Lezama-Ochoa N, Lopez J, Moreno G, Rojas-Perea S and Cronin MR (2024) Bycatch mitigation from the sky: using helicopter communication for mobulid conservation in tropical tuna fisheries. Front. Mar. Sci. 11:1303324. doi: 10.3389/fmars.2024.1303324
Received: 27 September 2023; Accepted: 14 February 2024;
Published: 04 March 2024.
Edited by:
Jon Brodziak, National Oceanic and Atmospheric Administration, United StatesReviewed by:
Jesse F. Senko, Arizona State University, United StatesNatascha Wosnick, Federal University of Paraná, Brazil
Copyright © 2024 Waldo, Altamirano-Nieto, Croll, Palacios, Lezama-Ochoa, Lopez, Moreno, Rojas-Perea and Cronin. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
*Correspondence: Jennifer L. Waldo, SmVubmlmZXIud2FsZG9Ab3JlZ29uc3RhdGUuZWR1
†ORCID: Jennifer L. Waldo, orcid.org/0009-0008-8519-7338
Marta D. Palacios, orcid.org/0000-0001-8466-6827
Nerea Lezama-Ochoa, orcid.org/0000-0003-3106-1669
Melissa R. Cronin, orcid.org/0000-0001-5315-8619