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Rings of Power: evidence of mud ring feeding performed by Guiana dolphins

Published online by Cambridge University Press:  18 September 2024

Julia C. Pierry Open the ORCID record for Julia C. Pierry [Opens in a new window] ,
Mariane B. S. Novelli ,
Caio N. Louzada  and
Emygdio L. A. Monteiro-Filho
Julia C. Pierry*
Affiliation:
Instituto de Pesquisas Cananéia (IPeC), Cananéia, São Paulo, Brazil Laboratório de Biologia e Ecologia de Vertebrados, Departamento de Zoologia, Universidade Federal do Paraná, Curitiba, Paraná, Brazil Programa de Pós-Graduação em Zoologia, Departamento de Zoologia, Universidade Federal do Paraná, Curitiba, Paraná, Brazil
Mariane B. S. Novelli
Affiliation:
Instituto de Pesquisas Cananéia (IPeC), Cananéia, São Paulo, Brazil Laboratório de Biologia e Ecologia de Vertebrados, Departamento de Zoologia, Universidade Federal do Paraná, Curitiba, Paraná, Brazil Programa de Pós-Graduação em Zoologia, Departamento de Zoologia, Universidade Federal do Paraná, Curitiba, Paraná, Brazil
Caio N. Louzada
Affiliation:
Instituto de Pesquisas Cananéia (IPeC), Cananéia, São Paulo, Brazil
Emygdio L. A. Monteiro-Filho
Affiliation:
Instituto de Pesquisas Cananéia (IPeC), Cananéia, São Paulo, Brazil Laboratório de Biologia e Ecologia de Vertebrados, Departamento de Zoologia, Universidade Federal do Paraná, Curitiba, Paraná, Brazil Programa de Pós-Graduação em Zoologia, Departamento de Zoologia, Universidade Federal do Paraná, Curitiba, Paraná, Brazil Departamento de Zoologia, Setor de Ciências Biológicas, Universidade Federal do Paraná, Curitiba, Paraná, Brazil
*
Corresponding author: Julia C. Pierry; Email: juliapierry@yahoo.com.br
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Abstract

To capture prey more efficiently, cetaceans can display a wide range of foraging tactics to separate individual prey. Barrier feeding tactics are performed to restrict prey movements, using natural and non-natural barriers and some species can even create barriers with their own bodies. Mud ring feeding has been observed in bottlenose dolphins in Florida Bay and in Chetumal-Corozal Bay, where ring-maker dolphins create ring-shaped mud plumes to encircle fish schools. Here, we document for the first time Guiana dolphins performing the mud ring feeding behaviour in the Cananéia estuarine system, in the southern portion of the state of São Paulo, Brazil. A total of 11 dolphins were recorded in four expeditions through aerial footage engaging in the behaviour. These findings expand our knowledge about the behavioural plasticity of the species and builds upon existing records of mud ring feeding behaviour in cetaceans.

Keywords

barrier feedingbehavioural plasticitybottlenose dolphincetaceansestuarine dolphinforaging tactics

Information

Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 104 , 2024 , e69
Copyright
Copyright © The Author(s), 2024. Published by Cambridge University Press on behalf of Marine Biological Association of the United Kingdom

Introduction

To capture prey more efficiently, cetaceans display a wide range of foraging tactics that seek to separate individual prey (Shane, Reference Shane, Leatherwook and Reeves1990; Nowacek, Reference Nowacek1999; Gubbins, Reference Gubbins2000; Monteiro-Filho, Reference Monteiro-Filho2008). Some species perform behaviours associated with habitat features, using them to restrict prey movement and block escape routes, such as bottlenose dolphins (Tursiops truncatus) that use estuarine mudflats to perform strand feeding behaviour (Hoese, Reference Hoese1971; Petricig, Reference Petricig1995; Silber and Fertl, Reference Silber and Fertl1995), or use shallow sand banks for crater feeding behaviour (Rossbach and Herzing, Reference Rossbach and Herzing1997).

Barrier feeding tactics can be performed using natural and non-natural barriers and some species may create the barriers themselves. Humpback whales (Megaptera novaeangliae) are well known for creating bubble barriers to corral or herd fish (Jurasz and Jurasz, Reference Jurasz and Jurasz1979; Hain et al., Reference Hain, Carter, Kraus, Mayo and Winn1982; Acevedo et al., Reference Acevedo, Plana, Aguayo-Lobo and Pastene2011). In some cases, individuals use their pectoral fins as a secondary barrier in combination with bubble barriers to prevent evasion by prey (Kosma et al., Reference Kosma, Werth, Szabo and Straley2019). Even in greater depths where barriers are absent, spinner dolphins (Stenella longirostris) and bottlenose dolphins can line up or swim in a circle using their bodies as physical barriers (Gazda et al., Reference Gazda, Connor, Edgar and Cox2005; Benoit-Bird and Au, Reference Benoit-Bird and Au2009).

In the Florida Keys, bottlenose dolphins have been observed creating linear or curvilinear mud plume barriers by moving their flukes in a downwards motion near the substrate, then lunging quickly into it to catch fish prey (Lewis and Schroeder, Reference Lewis and Schroeder2003). The same species has been observed performing mud ring feeding in Florida Bay and in Chetumal-Corozal Bay, where a ring-maker dolphin creates a circular ring-shaped mud plume, used to corral fish schools and capture them when they leap out of the mud ring and into the air (Torres and Read, Reference Torres and Read2009; Engleby and Powell, Reference Engleby and Powell2019; Ramos et al., Reference Ramos, Santoya, Verde, Walker, Castelblanco-Martínez, Kiszka and Rieucau2021).

The Cananéia estuary in southeastern Brazil holds a resident population of approximately 400 Guiana dolphins (Sotalia guianensis) (Mello et al., Reference Mello, Molina, Kajin and Santos2019), – a small delphinid species that occurs from Honduras (Edwards and Schnell, Reference Edwards and Schnell2001) to southern Brazil (Simões-Lopes, Reference Simões-Lopes1988), mostly inhabiting estuaries, bays, and inlets. This resident population from Cananéia is known for performing a wide array of foraging behaviours, such as using fixed manmade traditional fishing traps (i.e., cerco-fixo) to direct their prey (Monteiro-Filho, Reference Monteiro-Filho1995; Louzada, Reference Louzada2013), using the shoreline along sloping beaches to facilitate prey capture by herding (Monteiro-Filho, Reference Monteiro-Filho1995) and even using mangrove areas as a barrier-foraging tactic (Pierry et al., Reference Pierry, Morete, Monteiro-Filho and Teixeira2023).

Here, we document mud ring feeding by Guiana dolphins, a behaviour previously described only in bottlenose dolphins (Torres and Read, Reference Torres and Read2009; Engleby and Powell, Reference Engleby and Powell2019; Ramos et al., Reference Ramos, Santoya, Verde, Walker, Castelblanco-Martínez, Kiszka and Rieucau2021). We describe this behaviour for the first time, performed by Guiana dolphins in the Cananéia estuary, using unmanned aerial vehicle (UAV) imagery that allowed us to observe the behaviour in this species and compare it with that already described in bottlenose dolphins. We hypothesize that the habitats’ similarities and both species behavioural plasticity drove them to separately evolve the same behaviour, which optimized foraging efforts to capture prey more efficiently.

Materials and methods

The observations took place in the Cananéia estuarine system, located in the southern portion of the state of São Paulo, in southeastern Brazil (Figure 1). All observations occurred at the same place within the Cananéia estuary – in the north portion of Cardoso Island State Park. This specific area is characterized by shallow waters (approximately one metre deep) during low tide, partially protected due to the topography of the Cardoso Island with a large mangrove area, and for presenting a sequence of twelve fixed traditional fishing traps, spaced approximately 100 metres apart (i.e., cerco-fixo; Radasewsky, Reference Radasewsky1976). These traditional fishing traps are characterized by a long sequence of wooden sticks that form a longitudinal barrier from the coast towards the estuary, which direct the fish to the structure's circular edge, where the fish will be trapped in a net that covers the entire structure from the inside.

Figure 1.

Study area in Cananéia estuary, southeastern Brazil. Detail shows the exact place where the mud ring feeding behaviour was recorded for Guiana dolphins (Sotalia guianensis), with an aerial view of the area and of the cerco-fixo – a traditional fishing trap.

Half of our expeditions were vessel-based, and the other half land-based, totalling four expeditions. The first two observations were recorded in February 2023 as opportunistic events, during two vessel-based expeditions that were made to record Guiana dolphins in the region for a documentary television programme, which was achieved with the support of our research team. Subsequently we undertook two scientific expeditions in August 2023, both land-based, to document this novel behaviour. In these expeditions, two observers scanned the area from land for four-hour observation periods in each expedition, both with the naked eye and using binoculars to identify the presence of dolphins and assess group size and composition. When dolphins were located, we collected aerial imagery using an UAV (models DJI Mavic Pro and DJI Mavic Air 2) at a pre-established height range of 20 to 30 metres, under local and national licenses (CadGP n°: 057479/2023; SISBIO n°: 88901-1) following established flight protocols to record small cetaceans (Fettermann et al., Reference Fettermann, Fiori, Gillman, Stockin and Bollard2022; Aubin et al., Reference Aubin, Mikus, Michaud, Mennill and Vergara2023).

Results

In each of the four field expeditions we observed one group of dolphins performing mud ring feeding to trap and catch fish prey, in each case during mid to low tides. In total, 11 dolphins were observed exhibiting this behaviour, distributed in four small, cohesive groups, each recorded in a separate field expedition: one group was composed of two adults and the other three groups were each comprised of two adults and one calf. Almost seven minutes of aerial video data were recorded of mud ring feeding behaviour being performed by Guiana dolphins. Photo-identification images were not taken of the 11 dolphins, so it was not established whether these were 11 unique individuals or included repeat encounters of some of the same individuals.

The first observation consisted of a group of two adults that performed three mud ring behaviour sequences – two performed by both individuals and one performed by a single animal (Supplementary Movies S1; S2; S3). When in pairs, both dolphins acted as ring-makers, actively moving their flukes towards the substrate while swimming in a circular movement until the dolphin that initiated the behaviour closed the mud ring inside the mud trail created by the second dolphin, turning the final shape into a mud spiral (Figure 2A). Small fish were observed jumping out of the water to flee above the mud plume on one occasion (Figure 2B). The spiral-like mud trail was also observed when the behaviour was performed by a single dolphin (Figure 2C). Both individually and in pairs, after completing the mud ring, the dolphins turned their bodies quickly in a 180° movement, returning their rostrum to the ring centre or to the mud suspended by the ring formation and sometimes swimming thorough the mud, likely to catch fish separated from their school.

Figure 2.

Mud ring feeding behaviour performed by Guiana dolphins (Sotalia guianensis) in the Cananéia estuary, southeastern Brazil. In (A) two dolphins acting as the ring-maker with the final mud spiral shape; in (B) it is possible to observe small fish jumping above the mud on the left side of the mud ring (circled); in (C) the spiral-shaped mud created by a single dolphin that swam into the mud plume after creating it; (D) shows a mother-calf pair approaching the mud ring created by the escort adult; in (E) the escort adult just remade the mud ring while the mother (closest to the ring-maker) and calf both remain stationary at the mud plume (arrowed); and (F) illustrates both adults performing as ring-makers, with the mother-calf pair swimming in echelon formation and a fish school being encircled (circled). Photos A, B, C, E: Marcelo Ferri; photos D, F: Julia Pierry.

The remaining three observations were of groups with three individuals, each being a mother-calf pair accompanied by another adult and each group performed one mud ring behaviour sequence. On these occasions, the ring-maker role was taken by either both adults simultaneously or by the escort dolphin alone. In the latter case, the mother-calf pair quickly moved towards the mud ring to position themselves at the mud plume once the escort dolphin initiated it (Figure 2D; Supplementary Movie S4). In one of the two occasions in which the escort dolphin created the mud ring, it was necessary to remake the ring, as a reinforcement for the barrier created by the mud. Then, instead of searching for fish in the mud, both adults and the calf remained in a stationary position with the rostrum directed to the ring centre for over 15 s after the mud ring was remade (Figure 2E; Supplementary Movie S5).

When performed simultaneously, one adult initiated the mud ring, being immediately followed by the mother-calf pair that swam in the opposite direction with the mother also acting as a ring-maker, until meeting the first adult midway around the formed mud ring. In this case, the calf stayed close to the mother until the ring was closed (i.e., echelon swimming cf. Rautenberg and Monteiro-Filho, Reference Rautenberg, Monteiro-Filho, Monteiro-Filho and Monteiro2008; Teixeira et al., Reference Teixeira, Louzada, Meyer and Monteiro-Filho2018), then the calf swam alone in the interior of the ring while both adults swam through the mud ring formation chasing fish. A fish school was observed trapped inside the mud ring (Figure 2F; Supplementary Movie S6). In half of the observed cases, the mud ring behaviour was performed near the fixed traditional fishing traps (less than 1 metre away), which allowed the dolphins to pursue their prey both within the mud ring and between the mud ring and the fixed traps.

We refer to the behaviour described here in Guiana dolphins as mud ring feeding since it shares close similarities with the behaviour described in bottlenose dolphins from Florida Bay and Chetumal-Corozal Bay (Table 1) – mainly due to the circular shape created in the mud, similar substrate and habitat features, occurring in inner-basin mud banks and for being a cooperative foraging tactic, rather than an individual behaviour as described in mud plume behaviour (Torres and Read, Reference Torres and Read2009; Engleby and Powell, Reference Engleby and Powell2019; Ramos et al., Reference Ramos, Santoya, Verde, Walker, Castelblanco-Martínez, Kiszka and Rieucau2021). The depths were similar in all sites for both bottlenose and Guiana dolphins. The target prey in each case varied from exclusively mugilid fish in Florida and Chetumal-Corozal Bays to multiple species in the Florida Keys (Lewis and Schroeder, Reference Lewis and Schroeder2003). In our observations we were able to identify in two different expeditions that the target prey were mugilids (Mugil sp.), possibly white mullets (Mugil curema), according to reports by local fishermen of the most commonly caught fish in the fixed traps and by the identification of the species through our footage. A remarkable difference observed between species is that for Guiana dolphins the ring-maker role can be shared, with two individuals actively creating the mud ring at the same time, which does not occur in bottlenose dolphins.

Table 1.

Similarities between the mud ring feeding described here for Guiana dolphins to both mud plume and mud ring feeding described for bottlenose dolphins (Lewis and Schroeder, Reference Lewis and Schroeder2003; Torres and Read, Reference Torres and Read2009; Engleby and Powell, Reference Engleby and Powell2019; Ramos et al., Reference Ramos, Santoya, Verde, Walker, Castelblanco-Martínez, Kiszka and Rieucau2021)

Discussion

Our results support the hypothesis that environmental features may contribute to shape foraging behaviour adaptations for dolphins worldwide (Würsig and Pearson, Reference Würsig, Pearson, Yamagiwa and Karczmarski2014; Methion and Díaz López, Reference Methion and Díaz López2019). Both the shallow protected waters and prey behaviour could be factors driving the development of the same behaviour between two different species in geographically separated locations. Even with this preliminary assessment, our records contribute to the evidence for Guiana dolphin's behavioural plasticity (Monteiro-Filho, Reference Monteiro-Filho2008; Deconto and Monteiro-Filho, Reference Deconto and Monteiro-Filho2013; Leão et al., Reference Leão, Monteiro-Filho and Silva2016).

Within the same species, we see great variation in behaviours among different populations and even among individuals (Shane, Reference Shane, Leatherwook and Reeves1990; Nowacek, Reference Nowacek1999; Gubbins, Reference Gubbins2000; Sargeant and Mann, Reference Sargeant, Mann, Laland and Galef2009). The mean group size of Guiana dolphins in the Cananéia estuary is within the range of 1 to 3 individuals, larger groups commonly occurring when the smaller ones come together for specific and ephemeral circumstances, such as foraging tactics that benefit from a greater number of individuals working together (Monteiro-Filho, Reference Monteiro-Filho1991, Reference Monteiro-Filho1992). The small group size and composition of the Guiana dolphins observed performing mud ring feeding recurrently at the same site, and this being such a specific behaviour, can suggest that this tactic is performed by a subset of dolphins within this population. Yet, considering the numerous mud banks along the estuary and the wide occurrence of mugilids, this behaviour may not necessarily be restricted to this single location. Indeed, over more than forty years of study in the region, various researchers on our team have documented Guiana dolphins with patches of mud on their back and sides along the estuary. Also, our records only show the white mullet as the target prey, but the generalist diet of Guiana dolphins in estuarine regions and the diversity of similar prey species in the Cananéia estuary suggests the possibility of predation of a wider list of target species using this tactic (Cremer et al., Reference Cremer, Pinheiro and Simões-Lopes2012; Ferro de Godoy et al., Reference Ferro de Godoy, Mendonça and Andriolo2020; Teixeira et al., Reference Teixeira, Botta, Cremer, Marcondes, Pereira, Newsome, Daura-Jorge and Simões-Lopes2023).

As mud ring feeding behaviour depends on a muddy substrate to be performed, it is possible that this behaviour occurs in other populations in this species’ distribution, especially those that share a similar habit of residency, such as the Paranaguá estuary and the Caravelas River, on the south and northeast coast of Brazil respectively. Indeed, Guiana dolphins have already been observed with mud patches on their bodies in the Caravelas River, which has been suggested to be associated with bottom foraging behaviours (Rossi-Santos and Wedekin, Reference Rossi-Santos and Wedekin2006).

An important feature of the Cananéia estuary is the presence of fixed traditional fishing traps (cerco-fixo; Radasewsky, Reference Radasewsky1976). The fact that most of the mud rings registered were created near to these traps, may indicate the advantage of physical barriers to this behaviour. By using the cerco-fixo as an additional barrier with the mud ring, prey escape routes are reduced, enhancing both predation and cooperation between individuals, with an individual chasing the fish inside the mud ring while another chases them between the ring and the cerco-fixo wall.

Tool use in cetaceans can be defined as the use of either an object from their habitat or the manipulation of environmental features such as waves, bubbles, water jets and mud to achieve an objective, generally associated with foraging behaviours (Mann and Patterson, Reference Mann and Patterson2013). In addition to creating mud rings, bottlenose dolphins also use sponges and shells to facilitate foraging (Smolker et al., Reference Smolker, Richards, Connor, Mann and Berggren1997; Allen et al., Reference Allen, Bejder and Krützen2011; Krützen et al., Reference Krützen, Kreicker, MacLeod, Learmonth, Kopps, Walsham and Allen2014; Wild et al., Reference Wild, Hoppitt, Allen and Krützen2020). Other cetacean species such as humpback whales and orcas (Orcinus orca) have also been observed using the sediment as a tool to increase their foraging success (Hain et al., Reference Hain, Ellis, Kenney, Clapham, Gray, Weinrich and Babb1995; Rossbach and Herzing, Reference Rossbach and Herzing1997; Visser, Reference Visser1999). Social interactions between differently aged individuals during behaviours involving tool use in cetaceans may lead to observational learning and attempts of imitation by younger individuals (Galef and Giraldeau, Reference Galef and Giraldeau2001; Laland, Reference Laland2004; Kuczaj and Yeater, Reference Kuczaj and Yeater2006).

The calves observed along with adults during the mud ring behaviour were swimming in close proximity to their mothers which exposes them to this tactic that can eventually be used in later stages in their life (Link, Reference Link2000; Spinelli et al., Reference Spinelli, Nascimento and Yamamoto2002; Lodi, Reference Lodi2003; Monteiro-Filho, Reference Monteiro-Filho2008). Like many other specialized foraging behaviours, the mud ring feeding displayed by Guiana dolphins may be socially learned – i.e. maternally by vertical transmission rather than by a horizontal or oblique learning mechanism among individuals, since there was no evidence of multiple groups interacting during this behaviour (Nowacek, Reference Nowacek2002; Mann and Sargeant, Reference Mann, Sargeant, Fragaszy and Perry2003; Wells, Reference Wells, de Waal and Tyack2003; Whitehead et al., Reference Whitehead, Rendell, Osborne and Würsig2004; Krützen et al., Reference Krützen, Mann, Heithaus, Connor, Bejder and Sherwin2005; Bender et al., Reference Bender, Herzing and Bjorklund2009; Torres and Read, Reference Torres and Read2009). Another potential indicator of vertical social learning is the presence of infants even though the shallow water (<1 m) presents a risk of stranding to inexperienced calves (Rautenberg and Monteiro-Filho, Reference Rautenberg, Monteiro-Filho, Monteiro-Filho and Monteiro2008).

Our findings contribute to the already rich list of foraging behaviour displayed by Guiana dolphins and builds upon existing records of mud ring feeding behaviour in cetaceans. The fact that these behaviours are displayed by different delphinid species with a great geographic distance between them, demonstrates a strong adaptive behaviour that may increase the foraging success for both species.

Supplementary material

The supplementary material for this article can be found at https://doi.org/10.1017/S002531542400078X.

Data

The data that supports this finding is available online in the Supplementary materials section of this article.

Acknowledgements

We thank the Instituto de Pesquisas Cananéia (IPeC) for the logistical support. We also thank Marcelo Ferri from the Terra da Gente TV programme who graciously provided his aerial footage and Ivaldo Neves, a local fisherman who helped identify the fish species.

Author contributions

All authors designed the study, JP performed the research and wrote the first draft of the manuscript, JP and MN collected data, CL and EMF provided materials for data collection and accuracy and all authors contributed substantially to revisions.

Financial support

This research received no specific grant from any funding agency, commercial or non-profit sectors.

Competing interests

The authors declare none.

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Figure 0

Figure 1. Study area in Cananéia estuary, southeastern Brazil. Detail shows the exact place where the mud ring feeding behaviour was recorded for Guiana dolphins (Sotalia guianensis), with an aerial view of the area and of the cerco-fixo – a traditional fishing trap.

Figure 1

Figure 2. Mud ring feeding behaviour performed by Guiana dolphins (Sotalia guianensis) in the Cananéia estuary, southeastern Brazil. In (A) two dolphins acting as the ring-maker with the final mud spiral shape; in (B) it is possible to observe small fish jumping above the mud on the left side of the mud ring (circled); in (C) the spiral-shaped mud created by a single dolphin that swam into the mud plume after creating it; (D) shows a mother-calf pair approaching the mud ring created by the escort adult; in (E) the escort adult just remade the mud ring while the mother (closest to the ring-maker) and calf both remain stationary at the mud plume (arrowed); and (F) illustrates both adults performing as ring-makers, with the mother-calf pair swimming in echelon formation and a fish school being encircled (circled). Photos A, B, C, E: Marcelo Ferri; photos D, F: Julia Pierry.

Figure 2

Table 1. Similarities between the mud ring feeding described here for Guiana dolphins to both mud plume and mud ring feeding described for bottlenose dolphins (Lewis and Schroeder, 2003; Torres and Read, 2009; Engleby and Powell, 2019; Ramos et al., 2021)

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