acta ethol (2013) 16:9–19 DOI 10.1007/s10211-012-0132-2
ORIGINAL PAPER
Resource defence and dominance hierarchy in the boto (Inia geoffrensis) during a provisioning program Luiz Cláudio Pinto de Sá Alves & Artur Andriolo & Mark Bryan Orams & Alexandre de Freitas Azevedo
Received: 15 May 2012 / Revised: 10 July 2012 / Accepted: 23 July 2012 / Published online: 9 August 2012 # Springer-Verlag and ISPA 2012
Abstract Aggression is often utilised in intraspecific competition to establish and maintain dominance hierarchies in social mammals. Here, we determine if aggressiveness in conditioned botos (Inia geoffrensis) during interactions with humans under provisioning is influenced by the presence or absence of food rewards and if provisioning leads to the establishment of a dominance hierarchy among these generally solitary animals. Mean values of bites among the botos for sessions in which food rewards were delivered were significantly higher than sessions in which no food reward was delivered. No significant difference exists between the mean number of bites per individual during feeding sessions, but the mean number of bites increased L. C. Pinto de Sá Alves (*) : A. de Freitas Azevedo Programa de Pós-graduação em Meio Ambiente, Universidade do Estado do Rio de Janeiro, Rua São Francisco Xavier, 524/12005-F, Rio de Janeiro, RJ 20550-900, Brazil e-mail:
[email protected] L. C. Pinto de Sá Alves : A. Andriolo Instituto Aqualie, Rua Edgard Werneck, 428/32, Rio de Janeiro, RJ 22763-010, Brazil A. Andriolo Departamento de Zoologia, Instituto de Ciências Biológicas, Universidade Federal de Juiz de Fora, Campus Universitário, Juiz de Fora, MG 36036-330, Brazil M. B. Orams New Zealand Tourism Research Institute, School of Hospitality and Tourism, AUT University, Private Bag 92006, Auckland 1010, Aotearoa, New Zealand L. C. Pinto de Sá Alves : A. de Freitas Azevedo Laboratório de Mamíferos Aquáticos e Bioindicadores, Faculdade de Oceanografia, Universidade do Estado do Rio de Janeiro, Rua São Francisco Xavier, 524/4002-E, Rio de Janeiro, RJ 20550-013, Brazil
significantly with time when animals were not fed. Supplant behaviours were used as a non-harming alternative to bites. The botos’ provisioning is a case of instrumental conditioning, in which the conditioned botos expect to receive food from tourists, increasing competition among the animals when they are not fed. The provisioned botos exhibited an almost linear dominance hierarchy. Bites and supplant behaviours were used more frequently by dominant botos to prevent subordinates from obtaining food provisions. Interactions brought about by provisioning are likely to be harmful to the botos and potentially dangerous to humans. Keywords Amazon River dolphin . Artificial feeding . Central Amazon . Anavilhanas National Park . Agonistic behaviour
Introduction Aggressive behaviours in social animals generally involve some aspect of a threat or attack, normally directed toward another individual of the same species (Queiroz and Cromberg 2006), and bites are generally recognised as one form of aggression in a range of different animal species (e.g. Delahay et al. 2006; Forman and Brain 2006; Litvin et al. 2007; Martin and da Silva 2006). According to Martin and Bateson (1993) and Prakash et al. (1994), another form of aggression is supplant behaviour (in which a dominant individual displaces a subordinate individual from a site that the dominant individual then proceeds to occupy) (e.g. Barroso et al. 2000; Barton 1993; Croft 1980; Gil-Burmann et al. 1998; Orihuela and Galina 1997; Scott and Lockard 1999). Competition for scarce resources is often expressed among group-living mammals in agonistic dominance relationships (Samuels and Gifford 1997). Competitive hierarchies can occur when access to food resources is determined by the relative
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hierarchical position within a group (Webster and Hixon 2000). These hierarchies in turn determine an animal’s access to resources such as space and food (Wirtu et al. 2004), in which the higher-ranked individuals have more access to these resources but also spend more energy to maintain a high position. The Amazon River dolphin or boto, Inia geoffrensis (de Blainville, 1817), is the biggest fluvial dolphin. Inia appears to be tolerant of human activity and is occasionally observed in close proximity to boats, swimmers and fishers. In some cases, they have been known to seek out tactile contact with humans; for example, wild Inia are reported to have grasped fisherman’s paddles and rubbed against canoes, and some have become quite tame (Best and da Silva 1989). Botos are rarely seen in cohesive groups of more than three individuals, even though larger aggregations may be seen in feeding areas or when animals are involved in courtship and mating (Best and da Silva 1993); otherwise, they are usually solitary (Best and da Silva 1989). In Brazil, five cases of aggregations of wild botos becoming conditioned to human contact through food provisioning for tourism purposes have been observed in Amazonas State, Central Amazon (first author, pers. obs.). At Novo Airão City (02°37′13.7″S and 60°56′45.9″W), locals have regularly provisioned boto since 1998 from a floating restaurant/bar, and today, there are at least 13 individual conditioned botos (Alves et al. 2011). Orams (2002) showed that provisioned dolphins exhibit altered natural behavioural patterns and claimed that an increase in aggression can become a significant problem related to such provisioning. Previous genetic research on botos in this area (Gravena 2007) has confirmed that ten of the conditioned individuals being provisioned were males, and no female was registered in the area during that research. According to Martin and da Silva (2006), adult male botos are generally much more heavily scarred than adult females, probably due to inter-male aggression. Because most (if not all) conditioned botos are males, we expected the close interaction with humans as a means to acquire food to result in aggressive competition for these food resources. We also hypothesised that conditioned botos would employ social strategies in response to aggressiveness during provisioning activities. Our main objectives are to determine if aggressiveness among conditioned botos during interactions with humans is determined by the presence or absence of food rewards and to determine if provisioning leads to the establishment of a dominance hierarchy among those animals.
Materials and methods Study area This study was conducted at a floating restaurant (02°37′ 13.7″S and 60°56′45.9″W), located in Novo Airão city,
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Amazonas State, Brazil, in the Anavilhanas National Park (Fig. 1). Novo Airão is located on the southern banks of the Negro River next to the city of Manaus (the State Capital). Data were acquired by a single observer during two periods, from 20 May to 2 August 2008 and from 12 March to 9 May 2009, for a total of 134 days of observations. At this site, interactions with botos occur at a 7-m long, 11m wide section at the rear of the floating restaurant. This area also has two 4-m wide wooden platforms close to water level, separated by a 3-m submersed tree trunk, where people can access the water and touch the botos while feeding them (Fig. 2). During this study period, there was no regular provisioning schedule, and tourists could provision and interact with the dolphins at any time, every day of the week. Ad libitum observations During the first 7 days of observations, the ad libitum sampling (Altmann 1974) was used to identify the specific types of behaviour most suitable to achieve our objectives and how to collect the data, in addition to evaluating the sampling durations that would allow us to achieve our first main objective. The observer was positioned on the higher platform (approximately 1.5 m above the water level) to better observe the interactions. In particular, we focussed on access to provisioned food, defence of positions and food, as well as other indications of a dominance hierarchy and aggression. Observations were conducted daily between 08:00 h and 17:00 h from the rear part of the floating restaurant. Definition of study situations Feeding sessions were defined as when botos were in close proximity (within approximately 5 m) to the floating restaurant and were being offered food rewards by a tourist. Non-feeding sessions were defined as when botos were in close proximity to the floating restaurant but not being offered any food reward. In these cases, one tourist interacted with the dolphins similarly to those during the feeding session (for the entire observation periods, there was always a tourist trying to attract the animals by moving a hand and pretending to have a fish). Bite behaviour was defined as when a boto deliberately and assertively made physical contact with any part of another boto’s body using its teeth through an open mouth. The bite behaviour approach was defined as when, during sampling sessions, only bites occurred and were recorded. Supplant behaviour was defined as when a boto deliberately and assertively positioned its body to block, push or guide another boto or botos away from a feeding opportunity. The supplant behaviour approach was defined as when, during sampling sessions, supplants and bites occurred and were both recorded.
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Fig. 1 Above, left: Amazonas State in Brazil; above, right: Anavilhanas National Park in Amazonas State; below: Anavilhanas National Park in the municipalities of Manaus and Novo Airão and the interactions site, located in Novo Airão city
Bite and supplant behaviour approaches With the all-occurrences sampling method (Altmann 1974), we recorded all bite and supplant events among the botos
during 90-min-long sampling sessions, divided into three consecutive periods of 30 min (designated as periods 1, 2 and 3). Based on ad libitum observations, three periods of 30 min were considered sufficient to detect individual
Fig. 2 Left: the floating restaurant’s rear part in Novo Airão; Right: a bite during a tourist–boto interaction in Novo Airão
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behavioural alterations. In addition, it would be difficult to analyse longer sessions because tourists rarely interacted (especially feeding) continuously with the botos for longer periods. The total number of bites and supplants that occurred in each period was divided by the number of individuals present in the area (the same individuals were recorded during the entire period of each sampling session), resulting in the number of events (bites or supplants) per individual per period of time (bites or supplants/individual/ 30 min). Only interactions that occurred less than a maximum distance of 5 m from the wooden platforms at which provisioning occurred were recorded, as the animals rarely interacted with other individuals outside of these limits. Interactions with tourists generally occurred within a maximum distance of 1 m from the platform. All-occurrence sampling sessions were conducted from May to August of 2008. None of the botos were fed before morning observations, and they were fed in mornings before afternoon observations on only three of 15 occasions. They received less than 200 g of food per individual in the morning before these three sessions, which we considered insignificant in this context. Consequently, our analysis did not consider whether the botos had been fed in the morning. All observations were conducted when seven or fewer tourists were present on the platforms (but with no tourist in the water with the dolphins) and when there was only one tourist feeding or pretending to feed the botos (when numbers were higher, data were not collected). If feeding or feeding-like activities ceased for more than 5 min, the recording of data would stop, and the sampling session would be excluded from any analysis. Observations were conducted from 09:00 h to 10:30 h and from 14:00 h to 15:30 h. The acquired data were divided into two separate groups. Data analyses were conducted separately to allow the evaluation of bite behaviour without possible interference from supplant behaviour (bite behaviour approach). For sessions when both supplant and bite behaviours were observed, data were analysed together (supplant behaviour approach). The mean numbers of bites recorded during feeding and non-feeding sessions were compared between the bite behaviour and the supplant behaviour approaches to evaluate the impact of supplants on the frequency of bites (bite behaviour approach and supplant behaviour approach comparisons). Hierarchy study Only bites were considered for analysis in this study. Thirteen individual botos were identified based on unique markings and characteristics around the rostrum and head (they are known and named by the local people). Observations on pairs of individuals were conducted to establish the biter
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(actor) and the bitten (recipient). Observations were conducted daily between 08:00 h and 17:00 h, on both periods of the study (2008 and 2009) and were only interrupted while the observer was collecting data for the bite and supplant behaviour approaches. A sociometric matrix was completed, and the dyadic interactions were analysed for each pair of individuals. The direction and degree of one-sidedness of the bite behaviour was established for each pair. The number of times each individual acted as an actor and as a recipient within each dyad was used to create an individual dominance index inside the dyad (DID; based on Eden (1987)). The DID was determined by dividing the number of occurrences that the individual participated in as an actor by the total number of interactions (dominant–subordinate interactions) that the individual participated in within the dyad (DID0Wi/Ti, where: Wi0number of wins in interactions with opponent “i” and Ti0total number of interactions with opponent “i”). Only pairs that had at least ten recorded bite occurrences were considered for analysis using the DID. The actor was considered dominant in relation to the other individual if presenting a DID≥0.75, equal if DID ranged from 0.26 to 0.74 and subordinate if DID≤0.25. The categories are based on values used by Samuels and Gifford (1997), in which a dolphin was identified as a dominant member of a pair during months in which that individual won a preponderance (i.e., 76 %–100 %) of decided interactions with the opponent. A complementary dominance index, the individual dominance index inside the group (DIG), was calculated for each individual in relation to the group (based on Lehner (1996)). In this case, the DIG was calculated by dividing the total number of occurrences that the individual participated as an actor by the total number of interactions (dominant–subordinate) that the individual participated in with all other analysed individuals (DIG 0W/T, where: W0 number of wins and T0total number of dominant–subordinate interactions with other individuals), resulting in a value ranging from 0 (completely subordinate) to 1 (completely dominant). We were only able to collect enough data for ten individuals (because three individuals were only occasionally observed in the area), so the remaining three were excluded from these analyses. The hierarchical positions of all the ten individual botos were defined by the individual’s DID, DIG and ADIG (see below), enabling the calculation of the Landau’s index of linearity of the aggregation studied here, as presented the formula 3 by Lehner Pn (1996), by using 2 h ¼ 12 n n (where n 0 a¼1 ðVa fn 1g=2Þ number of animals in the group and Va 0number of animals that individual ‘a’ dominates). To build a unique hierarchical composition, we compared all dyads from the DIG results with those from the DID
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results, in order to evaluate all dyads resulting from the DIG that were consistent with the DID (an individual with a higher DIG within a dyad should be dominant or equal to the other individual, based on the DID). An adjusted dominance index inside the group (ADIG) was created when a boto did not meet the assumption of DIG based on DID. This index was the mean value of all DID values for that particular individual, resulting in a value from 0 (completely subordinate) to 1 (completely dominant). However, the ADIG takes into account the individual’s success with different opponents. The ADIG values were comparable to the DIG values of all other individuals. In addition, if an individual presented an undefined relation to another individual based on the DID but was hierarchically distant to this boto based on the DIG (at least a third individual with an intermediate value), it was considered dominant to that particular individual if presenting a higher DIG value and subordinate if presenting a lower value. Responses to bites The immediate behavioural responses of both actor and recipient in some bite events were also recorded, according to the sequence sampling method (Altmann 1974). Ethograms of responses to bite events were created for both actor and recipient. We considered the ending of a sequence when the observed dyad distanced from each other for a minimum distance of 1 m or when both started to engage in begging behaviour. Interactions in which dominant individuals were the actors were compared with interactions in which subordinates performed the bites. Observations were conducted daily from 08:00 h to 17:00 h and were interrupted only when the observer was collecting data for the previously described bite and supplant behaviours approaches. Supplementary supplant behaviour analysis Supplant events in which supplanters and all supplanted individuals were identified were compared with results from the hierarchy study, in order to evaluate the hierarchical position (dominant or subordinate) of both the supplanters and supplanted individuals.
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Results Ad libitum observations The presence of tourists in the rear section of the floating restaurant elicited continuous dolphin begging behaviour (head out of the water with an open mouth, based on criteria from Samuels and Bejder (2004)). Botos that were provisioned from the floating restaurant were frequently observed biting each other. On some occasions, some individual botos supplanted other botos present. On these occasions, these individuals chased these other botos from the feeding area with open jaws. The chaser would then return to the feeding area alone and resume begging for food. After some time (variable) or after the chaser received a piece of fish, the chaser would generally leave the area and the supplanted individuals would immediately return. Generally, the supplanter would swim in a wide circle (varied diameters) away from the feeding area and then return and repeat the supplanting behaviour. Individuals that acted as supplanters on some occasions were also observed in other situations where they did not show this kind of behaviour at all. Bite behaviour approach The mean number of botos attending a feeding session and a non-feeding session at the restaurant (3.92±1.44 and 4.06± 0.92 individuals, respectively) was not correlated with the number of bites per individual (described below) on either feeding (P00.206, rs0−0.375; N013) or non-feeding sessions (P00.216, rs0−0.327; N016). Mean values of bites for feeding (1.91±1.03 bites/individual/30 min) and nonfeeding (4.66±3.54 bites/individual/30 min) sessions were significantly different (P
