1. Introduction

Predators in marine ecosystems can affect community dynamics through diverse pathways, including top-down, bottom-up, and a variety of behaviour-mediated processes (Estes et al., 2016). Behavioural drivers of their ecological effects include foraging (or behavioural) facilitation (Kiszka et al., 2015, 2022). Thus, some species such as marine mammals and large teleosts (e.g., tuna; Family: Scombridae) can make previously unavailable resources accessible to other predators (Dill et al., 2003; Kiszka et al., 2015). Foraging facilitation could be critical for some predator species such as epipelagic seabirds in habitats where feeding opportunities are limited, particularly in oligotrophic ecosystems (Pitman & Ballance, 1992; Kiszka et al., 2015). However, the frequency, context, and importance of foraging facilitation remains poorly understood.

In the wider Caribbean region, marine predator communities in coastal ecosystems are diverse. However, their ecological roles and relationships are poorly understood. Coastal cetaceans such as common bottlenose dolphins (Tursiops truncatus) and several species of seabirds, such as double-crested cormorants (Nannopterum auritum), ospreys (Pandion haliaetus), and brown pelicans (Pelecanus occidentalis), frequently co-occur in estuaries and shallow lagoons (Jones & Gardner, 2004). The double-crested cormorant, hereafter cormorant, is one of the most abundant and broadly distributed seabirds in coastal and inland waters of North America, northern Central America, and parts of the Caribbean (Wires et al., 2001; Dorr et al., 2014). Cormorants are generalist predators feeding on a range of fish species in shallow waters, particularly in seagrass beds. They exhibit flexibility in resource preferences depending on habitat conditions and prey availability (Wilson & Wilson, 1988; Blackwell et al., 1997). They primarily target fish and invertebrates on the benthos or schooling species, mostly small fish (Blackwell et al., 1995; Gagnon et al., 2020). Bottlenose dolphins, the most common and widely distributed small cetacean in the coastal waters of North and Central America, inhabit a variety of coastal marine habitats and display a vast diversity of feeding tactics, particularly in inshore waters (Barros & Wells, 1998; Allen et al., 2001; Torres & Read, 2009). Both predators significantly overlap in their spatial distribution and show a strong preference for seagrass meadows as feeding grounds (Barros & Wells, 1998).

Bottlenose dolphins are distributed across the coast of Belize (e.g., Ramos et al., 2018; Castelblanco-Martinez et al., 2022; Ramos et al., 2024). The shallow lagoons of Turneffe Atoll host a resident population of bottlenose dolphins (Campbell et al., 2002; Dick & Hines, 2011; Ramos et al., 2018). Local dolphins in some areas of the atoll have been shown to feed primarily in habitats of mixed sand and seagrass substrate (Eierman & Connor, 2014). Cormorants are found throughout the coast of Belize including Turneffe Atoll (Russell, 1964; Mitten et al., 2004; Miller & Miller, 2006), and commonly feed in seagrass meadows.

Here we describe two observations suggesting that coastal bottlenose dolphins provide foraging opportunities to cormorants in Turneffe Atoll, in the offshore waters of Belize in the Caribbean Sea.

2. Methods

Field work was conducted in 2015 (June-August, November-December), 2016 (June-August) and 2017 (January). Boat surveys from small vessels (6-15 m long) were conducted from 0800 h to 1730 h and followed predetermined transects throughout areas of Turneffe Atoll to assess the occurrence, movements, and behaviour of bottlenose dolphins (Ramos, 2022). When dolphins were sighted, the vessel approached them moving slowly to within 30 m to collect photographs of both sides of each dolphin’s dorsal fin using a Canon EOS digital SLR camera with a telephoto lens (75-400 m).

Small drone flights to track and observe the behaviour of bottlenose dolphins were conducted with small multirotor DJI quadcopters. Two small (1240-1400 g) commercial multi-rotor drones were used: DJI Phantom 3 Professional (P3) and Phantom 4 (P4). Each model was equipped with a 4K high-definition camera mounted on a gimbal with 3-axis stabilization. The aircraft was flown over dolphins to conduct focal group follows in non-rainy conditions at wind speeds from 0 to 20 knots. If conditions allowed, the drone was manually launched from the boat. A ground station operator (usually the captain) held the aircraft overhead and the pilot launched it to an altitude of 20 to 50 m and navigated over dolphins, maintaining all animals present in the field-of-view of the camera. Aerial videos were filmed in 4K (3840 × 2160 dpi) for up to 24 min. The camera on each aircraft was angled downward at 45-90° angle towards focal animals. Relevant flight metrics (e.g., battery levels, distance to craft) and animal activity were monitored live through the streaming video in the DJI GO application on a mounted tablet (Samsung Galaxy 8, iPad 9). Efforts were made to fly the drone at a fixed position relative to the dolphin group. Dolphin behaviour was sampled until the animals went out-of-sight or the flight was ended because of low battery power, system errors, or poor weather conditions. Up to 6 flights were conducted per group follow of dolphins.

Videos were reviewed in VLC media player to describe the behaviours of cormorants and dolphins throughout these observations.

3. Results

On 36 days from 2015 to 2017, a total of 102 drone-assisted group follows were conducted. Videos in the presence of dolphins had a mean duration of 16.6 ± 2.1 min and ranged from 11.5 to 24.2 min. Follows resulted in 28.3 h (1697.1 min) of direct observations of dolphin activity.

We identified two different encounters during drone flights over dolphin groups on 15 July 2016 and 22 July 2016.

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Composite of surface images showing the two double-crested cormorants swimming near two coastal bottlenose dolphins during observation 1 on 15 July 2016. (A) Both cormorants followed the two dolphins at the surface as they fed in the seagrass substrate. (B) The dorsal fin of a resident dolphin TA025 (“Sawfin”) and (C) TA069 (“Propeller”). (D) Image of one of the double-crested cormorants in flight. Photo credit: Eric A. Ramos.

Citation: Behaviour 161, 6 (2024) ; 10.1163/1568539X-bja10269

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In observation 1 at 10:02 h on 15 July 2016, two cormorants were observed feeding in close proximity (between 0 and 4 m) to five bottlenose dolphins feeding in a seagrass meadow (Figure 1A–D). The observation extended over two consecutive drone flights of 13 min and 47 s and 16 min and 8 s, respectively. The five dolphins spent most of their time repeatedly diving and moving in multiple directions while orienting their rostrums towards the substrate and moving their rostrums up and down. Dolphins appeared to actively foraging by probing the seagrass. However, prey capture was not observed. Two cormorants spent most of the time in the vicinity of dolphins (2-6 m away), primarily following their movements (Figure 1A). Periodically, one or both birds would approach during more vigorous activity by one or more dolphins. Six times throughout the observation, a dolphin chased and attempted to bite a cormorant.

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Aerial drone observations of bottlenose dolphins feeding near double-crested cormorants (white circles) in the shallow lagoon waters of Turneffe Atoll in Belize in the Caribbean Sea. Videos were acquired with a DJI Phantom 4 Pro flown over dolphin groups. (A) Map depicting the movement of the dolphin group in this predominantly seagrass habitat. The track is based on dolphin group position every 10 s. (B) One double-crested cormorant followed the dolphins as they travelled between feeding sites. (C) The two birds then followed the foraging dolphins at the surface and underwater as they fed in the seagrass substrate. (D) In several instances, a single dolphin chased the cormorant and attempted to bite it. (E) Attempts from an individual dolphin caused the bird to take flight. Photo credit: Eric A. Ramos.

Citation: Behaviour 161, 6 (2024) ; 10.1163/1568539X-bja10269

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In observation 2 at 17:03 h on 22 July 2016, two cormorants were observed following a group of five bottlenose dolphins (Figure 2A-C) for 17 min and 32 s. Prior to this observation, the same dolphins travelled in areas of mixed seagrass/sandy bottom habitat, repeatedly engaging in bouts of bottom foraging then traveling (Figure 2A). Cormorants were observed following the dolphins as they were foraging in different areas, flying when dolphins swam quickly and swimming if the dolphins moved slower (Figure 2A). Similar to observation 1, both birds were observed swimming closely to the dolphins as they foraged near the bottom on a dense seagrass patch. At 17:07 h, a dolphin turned towards the bird and approached quickly, displaying open-mouth behaviours, and appearing to attempt to bite the bird, causing the cormorant to take flight (Figure 2D-E). Individual dolphins were observed capturing prey as they travelled to other areas where they bottom fed, however, the animal could not be clearly seen, and we could not identify the species.

In seven instances across both observations, dolphins briefly chased a cormorant with open mouth, suggesting an aggressive response of the dolphins (Figure 1D-E).

4. Discussion

In this study, we report brief observations suggesting that bottlenose dolphins provide foraging opportunities for double-crested cormorants at Turneffe Atoll. Although several species of cormorants display kleptoparasitism towards cons- and heterospecifics (e.g., Mahendiran & Urfi, 2010), it appears that cormorants take advantage of foraging bottlenose dolphins displacing prey, allowing the former to locate benthic or benthopelagic prey. However, this form of foraging association does not appear to be kleptoparasitic, as cormorants do not seem to take individual prey targeted by dolphins. Since dolphins exhibit agonistic responses to the presence of cormorants, foraging benefits to cormorants seem to offset the risk of being bitten or killed by dolphins. Higher prey detection capabilities in bottlenose dolphins might be the primary driver of these commensal associations that have been reported between cetaceans and seabirds in a range of ecosystems and contexts (for a review, see Kiszka et al., 2015, 2022).

Individual dolphins were observed capturing prey as they travelled to other areas where they forage on the seagrass meadows, and nearby dolphins sometimes pursued fish driven out of the seagrass by a different dolphin. However, we could not identify the prey fish species being pursued by dolphins or cormorants. At Turneffe, they are suspected to prey on small fish species, such as yellowfin mojarra (Gerres cinereus), snappers (Family: Lutjanidae), and a variety of smaller fin fish (Grigg & Markowitz, et al., 1997; Eierman & Connor, 2014). Eierman & Connor (2014) found dolphins at Turneffe preferentially forage in edge habitats, at the interface between seagrass and sandy bottoms. Overall, foraging with bottlenose dolphins may provide advantages to cormorants by most likely enhancing feeding rates.

These interactions have not been documented before at this site despite more than 20 years of studies of dolphins in this lagoon (Grigg & Markovitz, 1997; Campbell et al., 2002; Ramos et al., 2018, 2022; Castelblanco-Martinez et al., 2022). Examining the context-dependence and importance of these interactions is important to unravel the ecological impacts that small cetaceans have, not only as predators and prey, but also as foraging facilitators for other predators. Future research will focus on investigating the feeding rates of cormorants in association with bottlenose dolphins or not, particularly to further quantify the energetic costs of foraging in both situations. This research is important in the light of ongoing declines and recovery of certain predator species due to anthropogenic impacts, and to unravel the roles and importance of these animals in marine ecosystems.