Journal of Ethology

, Volume 34, Issue 3, pp 299–307 | Cite as

Infanticide in the Indo-Pacific humpback dolphin (Sousa chinensis)

Article

Abstract

Infanticide has been observed in several mammalian taxa and studied in considerable detail in carnivores and primates. Although reported previously in cetaceans, known cases are few and their socio-behavioral context remains poorly understood. We report here on three cases of social coercion directed at mother-neonate pairs of Indo-Pacific humpback dolphins (Sousa chinensis) in the Pearl River Estuary, southeast China. Two of these cases resulted in confirmed infanticide. To aid the interpretation of our field observations, we refer to the results of necropsies of calf carcasses stranded and recovered in our research area between 2003 and 2012, which indicate that in several cases the main cause of death of stranded calves was asphyxia resulting from blunt-force trauma. This is consistent with the aggressive behaviors seen during our field observations. We conclude that male infanticide is the most plausible interpretation of the observed behaviors, never previously reported for the genus Sousa, while the calf-directed aggression is likely a result of socio-sexual harassment by males as part of their reproductive strategy.

Keywords

Sexual coercion Sexual selection Sexual conflict Pearl River Estuary Cetaceans—dolphins 

Introduction

Killing of dependent infants by conspecific males, referred to as “male infanticide,” represents an explicit example of sexual conflict, which arises when the reproductive strategies of one sex impose fitness costs on the other (Trivers 1972; Hrdy 1979). Among mammals, it is notably more common in species characterized by prolonged infant dependency (van Schaik 2000b; Wolff and Macdonald 2004) and has been studied in considerable detail in primates (e.g., van Schaik 2000a; Palombit 2012; Yamagiwa et al. 2014) and carnivores (e.g., Packer and Pusey 1984; Pusey and Packer 1994), with the well-documented infanticide in lions frequently featured in textbooks of behavioral ecology (e.g., Davies et al. 2012). As the number of mammalian long-term field studies increases so does the number of reported cases of infanticide (Kappeler and Van Schaik 2004), with primates alone providing direct evidence of male infanticide in 56 populations of 35 species or, if indirect evidence is included, 80 populations of 51 species (Palombit 2012). In non-seasonal breeders or species with an inter-birth interval greater than the period between breeding seasons, infanticide can markedly accelerate a female’s return to estrus, which increases the probability of infanticidal males gaining subsequent sexual access to the mothers. Consequently, males are thought to be the primary perpetrators and beneficiaries of infanticide due to sexual selection and resource competition (Hrdy 1979; Glass et al. 1985; van Schaik 2000a; Palombit 2012).

In slow reproducing animals, even relatively low levels of infanticide can exert strong selection pressures (Hrdy 1979; Yamamura et al. 1990; van Schaik et al. 2004), hence various behaviors of females are hypothesized to function as counterstrategies to male infanticide. Detailed studies of primates indicate that the perpetrators are generally unrelated to the infants they attack (van Schaik 2000a; Palombit 2012). It is widely accepted, therefore, that females’ promiscuous mating with multiple males, extended mating periods and postconception mating, function to establish a non-zero probability of relatedness to their potential offspring in as many potentially infanticidal males as possible, i.e., making paternity unclear. At the same time, increased gregariousness of nursing females facilitates maternal vigilance and coalitionary social defense (Hrdy 1979; Pusey and Packer 1994; Wolff and Macdonald 2004; Palombit 2012). These behaviors provide a compelling indication that infanticide is an important factor contributing to the evolution of male-female bonds in the context of reproductive strategies of social mammals (Ebensperger 1998; Palombit 2000).

In cetaceans, infanticide was first reported in the late 1990s based on the observations of common bottlenose dolphins (Tursiops truncatus) off the northeast coast of Scotland (Patterson et al. 1998), which supported an earlier suggestion by Connor et al. (1996) that the high frequency of mating in Indo-Pacific bottlenose dolphins (Tursiops aduncus) could be a female strategy that reduces the risk of male infanticide. Two decades later, observed and inferred cases of infanticide in dolphins remain few and mostly anecdotal (Patterson et al. 1998; Dunn et al. 2002; Kaplan et al. 2009; Nery and Simão 2009; Robinson 2014). However, while male coercion towards estrous females has been interpreted as male sexual competition for receptive females (Connor et al. 2000a; Scott et al. 2005), calf-directed aggressive behavior suggests that some males may have infanticidal tendencies (Robinson 2014). As in lions and many primates, where the loss of a dependent young accelerates the resumption of ovarian cycling of the mother (Pusey and Packer 1994; van Schaik 2000a; Palombit 2012), female bottlenose dolphins become attractive to males within days of losing a calf, while otherwise they typically calve every 2–4 years (Connor et al. 1996). Promiscuous mating and formation of nursery groups may function as infanticide counterstrategies adopted by female cetaceans, along with the counter-predation function of the latter (Clapham and Palsbøll 1997; Connor et al. 2000b; Gowans et al. 2008).

The Indo-Pacific humpback dolphin (Sousa chinensis), hereafter referred to as humpback dolphin, is an obligatory inshore species that inhabits shallow-water habitats of Southeast Asia, from the east coast of India to central-east China (Jefferson and Rosenbaum 2014). In this report, we describe three cases of social coercion and calf-directed aggression in humpback dolphins seen in the Pearl River Estuary (PRE), southeast China. Two of these cases resulted in the confirmed death of a dependent young. To aid the interpretation of our field observations, we refer to the results of necropsies of stranded calf carcasses collected in the PRE between 2003 and 2012. We conclude that male infanticide is the most plausible interpretation of the observed behaviors, never previously reported for the genus Sousa.

Materials and methods

Field observations

Since mid-2010, regular photo-identification boat surveys were conducted in waters of the PRE (Fig. 1) as part of a multi-year photographic identification mark-recapture study (Karczmarski and Wu, study in progress; Karczmarski et al. 2016). High-quality images of the dorsal fin and dorsal ridge of dolphins were collected using professional digital cameras (Canon 1D series) with 100- to 400-mm image-stabilized lenses following a similar field protocol to that described in Karczmarski et al. (2005). Video footage of dolphin behavior was collected opportunistically, to aid focal observations and photographic data. Whenever vigorous intra- or inter-group interactions were seen, they were video recorded.
Fig. 1

Geographic locations of three cases of calf-directed aggression carried out by all-adult groups of Indo-Pacific humpback dolphins in the Pearl River Estuary (PRE) in 2011 and 2012

Dolphins were classified into five age classes (neonate, calf, juvenile, sub-adult and adult), based on neonatal features, relative body length and girth, and pattern of pigmentation (Jefferson 2000; Jefferson and Rosenbaum 2014). The sex of individuals was determined from photographs of the genital area of individually distinctive dolphins or, in some cases and for females only, from photographically documented adult-calf association (presumed mother-calf pairs) seen on several consecutive sightings of that specific adult individual.

Aggressive and coercive behaviors were classified as “sandwiching,” “ramming” and “tossing,” similarly as described in several other studies (Ross and Wilson 1996; Wedekin et al. 2004; Ford et al. 2005, Barrett-Lennard et al. 2011); see Table 1 for details. Group association data (courtesy of ongoing photo-identification research; L. Karczmarski and Y. Wu, study in progress) were used to assess the association pattern among the involved individuals.
Table 1

Aggressive and coercive behaviors exhibited by all-adult groups, directed at adult-neonate pairs of Indo-Pacific humpback dolphins, seen on three occasions in the Pearl River Estuary (PRE) in 2011 and 2012

Behavior

Description

Ramming

Hitting the target individual with the rostrum or torso, usually after sudden acceleration, frequently performed by several perpetrators simultaneously or in succession and repeated several times. Ramming may cause bilateral hematomas and rib fractures

Tossing

Hitting and lifting the target individual (neonate or calf) out of the water with the rostrum, torso or fluke, at times tossing the target completely into the air. Tossing may cause serious rib fractures, contusion and hemorrhage

Sandwiching

Surrounding the target (here, the adult-calf pair) and limiting its maneuverability by constricting it between the flanks of two or more perpetrators, usually followed by ramming or biting

Summary of necropsies

Reports of necropsies performed on calf carcasses stranded in the PRE between 2003 and 2012 were inspected for indications of whether calf-directed aggression may have contributed to death. All necropsies followed a standard dissection and sampling protocol, as given in Geraci and Lounsbury (2005), and used similar postmortem descriptors as in other known cases of infanticide in dolphins (Patterson et al. 1998; Dunn et al. 2002).

Results

Field observations

Case 1

On 19 October 2011 (Fig. 2) an adult humpback dolphin was seen in association with a male neonate and was surrounded by 11 other adults; focal observations and video recording began at 1509 hours. For the next hour, the 11 adults were seen harassing the adult-neonate pair in an apparently coordinated manner, with two perpetrators sandwiching the target while others rammed and separated the neonate from the accompanying adult and occasionally tossed the neonate out of the water. The accompanying adult was seen repeatedly altering its speed and reorienting into different echelon positions with the neonate, occasionally charging against the perpetrators. Over the course of an hour, this apparent defensive response became gradually less vigorous, while the neonate began showing decreased vitality, eventually requiring support to stay afloat. The death of the neonate was confirmed at 1611 hours with the assistance of close-up video footage. Following the neonate’s death, the accompanying adult carried the carcass on its rostrum and repeatedly blocked the perpetrators (and the research vessel) from reaching the dead neonate.
Fig. 2

The sequence of calf-directed aggression perpetrated by an all-adult group of Indo-Pacific humpback dolphins in the PRE on 19 October 2011: a one of the perpetrators rises partially out of the water and slaps the neonate with its front upper body and rostrum, b the adult accompanying the neonate hits back at one of the perpetrators, c one of the perpetrators lifts the neonate onto its head to toss it into the air, d the adult-neonate pair sandwiched between two perpetrators, e the neonate tossed out of the water by one of the aggressors, f the adult-neonate pair again sandwiched by the perpetrators

Case 2

On 28 September 2012 (Fig. 3) an adult accompanied by a neonate in echelon position was seen sandwiched by three other large individuals, two adults and one sub-adult. The observation began at 1403 hours and lasted 30 min. The adult-neonate pair continued to travel in a well-defined direction, with the adult effectively blocking the three other large individuals from direct contact with the neonate by altering the echelon position. The seemingly aggressive-defensive interactions continued in a manner similar to that in case 1, but with less intensity as only three perpetrators were present. Video footage showed that by the end of our focal follow, the neonate remained strong and capable of fast travel, while the accompanying adult remained effective in defending against the harassment.
Fig. 3

The sequence of calf-directed aggression perpetrated by an all-adult group of Indo-Pacific humpback dolphins in the PRE on 28 September 2012: a two perpetrators sandwich the adult-neonate pair; b the adult accompanying the neonate repositions itself and the neonate, preventing the perpetrators from direct access to the neonate; c one of the perpetrators rams the neonate from underneath with it rostrum and lifts the neonate partially out of the water; d the adult accompanying the neonate rams one of the perpetrators while it tosses the neonate partially into the air; e the adult-calf pair flanked by two aggressors; f the neonate lifted partially out of the water by one of the perpetrators, just before being tossed into the air

Case 3

On 12 October 2012 (Fig. 4) a high-speed chase was seen, involving an adult-neonate pair and three other adults. The three perpetrators sandwiched and rammed the pair, and occasionally tossed the neonate out of the water. The adult accompanying the neonate was seen frequently changing its speed and position in apparent attempts to block the neonate from aggressive attacks. The observation began at 0957 hours and lasted 30 min, by which time the neonate showed decreasing vitality, manifested in shorter and weaker surfacing and reduced swimming speed, followed by a further increase in the frequency of attacks by the perpetrators. The subsequent death of the neonate was confirmed with the aid of video footage and photographic record, but the carcass was not recovered.
Fig. 4

The sequence of calf-directed aggression perpetrated by an all-adult group of Indo-Pacific humpback dolphins in the PRE on 12 October 2012: a the adult accompanying the neonate blocks one of the perpetrators from approaching the neonate, b one of the perpetrators swims underneath the neonate and attempts to lift it out of the water, c another perpetrator rams the neonate from one side, d one of the perpetrators attempts to press against the neonate and its accompanying adult, e the adult-calf pair flanked by two aggressors, f the adult accompanying the neonate rams one of the perpetrators to regain the neonate

Summary of necropsy data

Of the 73 stranded carcasses of humpback dolphins that were recovered between 2003 and 2012, twenty-five (34.2 %) were calf carcasses. There was a notable sex bias towards male calves (1.5:1) compared to the overall sex ratio of all stranded dolphins (1.16:1). Gross necropsy findings indicate chest subcuticular contusions, rib fractures, and abnormal hemorrhage as the primary injuries (Table 2). In three cases (12 %), the cause of death of stranded calves was diagnosed to be asphyxia resulting from blunt-force trauma (Fig. 5), which is consistent with the aggressive behaviors seen during our field observations.
Table 2

Results of necropsies of Indo-Pacific humpback dolphin calves stranded in the PRE between 2003 and 2012

No.

Length (cm)

Sex

Stranding date

Condition code

Epidermic injury

Subcuticular contusion

Skeletal fracture

Abnormal hemorrhage

Soft tissue laceration

SC05

115

6 August 2004

4

NE

NE

N

NE

NE

SC09

103

10 June 2005

4

NE

NE

N

NE

NE

SC10

103

28 July 2005

4

NE

NE

N

NE

NE

SC16

116.5

7 August 2007

4

NE

NE

N

NE

NE

SC25

110

4 February 2009

2

NE

N

N

Hemothorax, lung/liver hemopexis

N

SC31

114

12 April 2009

3

NE

NE

N

NE

NE

SC30

113

22 May 2009

3

NE

NE

N

NE

NE

SC32

107

28 October 2009

3

NE

N

N

N

N

SC39a

79.5

25 April 2010

3

N

Dorsal

N

Lung hemopexis

N

SC40a

118

16 July 2010

3

N

Abdominal

rib (#2–5)

Hemothorax

N

SC41

109

22 July 2010

4

NE

NE

N

Hemothorax

N

SC43

106

5 September 2010

4

NE

NE

rib (#1, 2, 10)

NE

NE

SC45

113.5

1 December 2010

2

NE

N

N

Hemothorax, lung hemopexis

N

SC46

113

2 January 2011

2

NE

N

N

Hemothorax, lung hemopexis

N

SC51

115

19 August 2011

4

NE

NE

N

NE

NE

SC52

117

10 September 2011

4

NE

NE

N

Hemoperitoneum

N

SC53

107.5

14 September 2011

2

N

N

N

Hemoperitoneum, heart/lung hemopexis

N

SC55

115.8

3 October 2011

4

NE

NE

N

NE

NE

SC56

106

4 January 2012

2

N

N

N

Lung hemopexis

N

SC57a

105

16 January 2012

2

N

Pectoral

rib (#3–5)

Lung hemopexis

N

SC59

107

30 May 2012

3

Biting scar

Pectoral

N

N

N

SC63

109

24 July 2012

4

NE

NE

rib (#1–3)

NE

NE

SC66

89

20 September 2012

2

NE

NE

N

NE

NE

SC69

79.5

25 September 2012

2

NE

NE

N

NE

NE

SC71

103

7 October 2012

4

NE

NE

N

NE

NE

Carcass condition: live stranded (1), fresh (2), moderately decomposed (3), highly decomposed (4), unrecognizable (5)

NE No examination, N Nothing abnormal detected

aDeath was diagnosed to result from blunt-force trauma

Fig. 5

Images taken during a necropsy of a stranded calf of the Indo-Pacific humpback dolphin where the cause of death was diagnosed to be blunt-force trauma; a subcuticular contusion on the left thorax, b rib fracture (nos. 3–5), c hemothorax with severe exudation

Discussion

The three cases of calf-directed aggression seen in the PRE in 2011 and 2012 resulted in two cases of confirmed infanticide. The pattern of pigmentation and relative body size indicated that, with the exception of one sub-adult, all other perpetrators in these three cases were adults (Supplementary Material S1). None of these perpetrators had been seen in association with a calf or neonate either before or after the encounters described here (Table 3), suggesting that they may all have been males. On the contrary, two of the three adults that formed the adult-calf pairs (case 1 and 3) had been seen in association with a neonate/calf prior to the encounters described here, and the accompanying adult in case 2 continued to be seen in association with a calf in the months following the coercive incident (Table 3). Furthermore, 25 months after the infanticide described in case 1, the adult defending the neonate was seen with a new calf (Table 3). These observations suggest that all three adults that formed the adult-calf pairs were females, likely mothers of the accompanying neonates. In contrast, the calf-directed aggression may have been carried out by all-adult male groups. Decade-long stranding data suggest that these may have not been isolated cases.
Table 3

Summary of individual sighting histories, between mid-2010 and mid-2015, of Indo-Pacific humpback dolphins involved in three cases of calf-directed aggression observed in the PRE in 2011 and 2012

Event

Date

Individual identity

Presumed sex

Sightingsa

Sightings with calfa

Before

Total

Before

After

Total

Case 1

 

#0619

Female

3

5

1

1

3

19 October 2011

#0049

Male

8

14

0

0

0

 

#0112

Male

28

34

0

0

0

 

#0153

Male

3

5

0

0

0

 

#0325

Male

3

8

0

0

0

 

#0402

Male

4

22

0

0

0

 

#0612

Male

4

5

0

0

0

 

#0614

Male

15

23

0

0

0

 

#0615

Male

1

2

0

0

0

 

#0616

Male

1

20

0

0

0

 

#0617

Male

0

6

0

0

0

 

#0618

Male

0

6

0

0

0

Case 2

28 September 2012

#0357

Female

5

14

0

2

3

 

#0365

Male

5

13

0

0

0

 

#0441

Male

4

28

0

0

0

 

#0482

Male

9

21

0

0

0

Case 3

12 October 2012

#a0041

Female

15

52

3

0

4

 

#a0126

Male

6

30

0

0

0

 

#a0127

Male

2

35

0

0

0

 

#a0128

Male

0

13

0

0

0

aSightings before and after the three encounters described here

Individual sighting histories (L. Karczmarski and Y. Wu, study in progress) indicate no stable or preferred grouping among the perpetrators. Similarly, although some of the perpetrators had been seen in association with the presumed mothers prior to, and after, the encounters described here, these interactions were infrequent and casual; e.g., two of the perpetrators and the presumed mother seen in case 3 were seen together in the same group 2 days prior to the infanticide; and two of the perpetrators and the presumed mother from case 2 were seen in a loose foraging aggregation 9 months after the coercive incident described here. All presumed mothers displayed higher site fidelity than any of the perpetrators.

Central features of infanticide are variability and conditionality (van Schaik and Janson 2000); e.g., it is perpetrated by some but not all males, suggesting it to be a facultative reproductive strategy where the relative benefits vary with conditions, such as the number of estrous females, the ages of infants and other aspects of group dynamics (Palombit 2012). Infanticidal tendencies in males and resulting female counterstrategies in humpback dolphins may be driven by similar mechanisms to those in other fission–fusion mammalian groups. Male Indian Ocean humpback dolphins (Sousa plumbea) are thought to favor searching for receptive females, while nursing females display stronger site fidelity (Karczmarski 1999) to limited and patchily distributed preferred inshore habitats (Karczmarski et al. 2000) and form dynamic but often behaviorally well-coordinated nursing groups (Karczmarski et al. 1997). Coercive and herding behavior, with three adult individuals (one confirmed male and two presumed males) herding and mating with a female was also seen in shallow coastal habitats off Inhaca Island, Mozambique (L. Karczmarski, personal observation).

The male reproductive behavior observed in Indian Ocean humpback dolphins may well apply to Indo-Pacific humpback dolphins. Although no stable male–male alliances or coercive consortiums [as described for some other coastal dolphins (e.g., Connor et al. 1992, 2000a)] have been seen in the PRE, both the mate-searching behavior and potential tendency for occasional herding of females could be triggers for what appeared to be socio-sexual grouping of males and their aggressive behavior. The reproductive characteristics of female humpback dolphins, such as the lack of distinct seasonal ovarian cycling, the length of their gestation period, and long dependency of the calf (Karczmarski 1996; Jefferson 2000; Brook et al. 2004), make receptive mothers and dependent calves more vulnerable to such socio-sexual harassment.

In several primate species, there are well-documented cases of infanticidal attacks by extra-group males or all-male bands that target in particular mothers with infants (Palombit 2012). Interestingly, in one such case, in the chimpanzees (Pan troglodytes) of the Mahale Mountains, Tanzania, an overrepresentation of male infants among the victims (Kawanaka 1981; Hiraiwa-Hasegawa and Hasegawa 1987) is similar to that observed for humpback dolphins in the PRE. For the Mahale chimpanzees, however, this male bias becomes far less apparent when overall sex ratio at birth is considered (Nishida et al. 2003). No such verification is currently possible for the PRE humpback dolphins due to the paucity of field data.

In summary, we suggest that the observed infanticide in the PRE humpback dolphins is a result of socio-sexual harassment by males as part of their reproductive strategy. The death of an infant disrupts its mother’s socio-reproductive state and likely terminates her postpartum amenorrhea. Given the conservation status and current population trend of the PRE humpback dolphins (Huang et al. 2012; Karczmarski et al. 2016), such behavior may contribute to the high neonatal mortality rates observed in the PRE (Jefferson et al. 2006, 2012). However, as knowledge on the reproductive strategies of these dolphins is meager, and evidence from the field is notoriously difficult to obtain, more in-depth studies across several dolphin species is needed to better understand how infanticide and sexual harassment act as selection pressures on delphinid socio-sexual strategies.

Notes

Acknowledgments

This work is part of a larger-scale study supported by funding from the Research Grants Council of Hong Kong (GRF grants HKU768110M, HKU768913M and HKU17100015M), the National Natural Science Foundation of China (Grant Nos. 41276147 and 41576128), the Ocean Park Conservation Foundation Hong Kong and the Sousa chinensis Conservation Action Project of the Administration of Ocean and Fisheries of Guangdong Province, China. We thank Yuen-Wa Ho, Scott Y. S. Chui, Shiang-Lin Huang and Carmen K. M. Or for comments on an earlier draft of the manuscript, and Yingku Wang, Wenhua Liu, and laboratory staff at Sun Yat-sen University for their contribution to postmortem analyses.

Supplementary material

10164_2016_475_MOESM1_ESM.jpg (3.9 mb)
Supplementary material S1. Photo-ID images indicating the age of all individuals involved in the three cases of calf-directed aggression in Indo-Pacific humpback dolphins seen in the Pearl River Estuary in 2011 and 2012. In this species, the pattern of pigmentation changes with age, from dark gray at birth to light gray as juveniles and mottled or light pink as adults (for details see Jefferson 2000, Jefferson et al. 2012). White ID numbers on black background indicate the presumed mothers and black ID numbers on white background depict the perpetrators. One of the perpetrators was a large sub-adult and all other individuals were adults (JPEG 3993 kb)

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Copyright information

© Japan Ethological Society and Springer Japan 2016

Authors and Affiliations

  1. 1.South China Sea Bio-Resource Exploitation and Utilization Collaborative Innovation Center, School of Marine SciencesSun Yat-Sen UniversityGuangzhouPeople’s Republic of China
  2. 2.The Swire Institute of Marine Science, School of Biological SciencesThe University of Hong KongShek OHong Kong

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