Biology, ecology and anthropogenic threats of Indo-Pacific bottlenose

dolphins in east Africa

Omar A. Amir

Department of Zoology

Stockholm University 2010

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Biology, ecology and anthropogenic threats of

Indo-Pacific bottlenose dolphins in east Africa

Doctoral dissertation 2010

Omar A. Amir Department of Zoology Stockholm University SE-106 91 Stockholm Sweden

©Omar A. Amir, Stockholm 2010

ISBN 978-91-7447-002-4

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Dedicated to my parents, wife and children

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ABSTRACT This thesis examines the biology, ecology and anthropogenic threats of Indo-Pacific bottlenose dolphins (Tursiops aduncus) off Zanzibar, Tanzania, based on research conducted and samples collected between 2000 and 2008. Distribution and occurrence are described based on incidental catches (bycatch) in gillnet fisheries. Biology and ecology are examined by ageing and studying the reproductive biology and stomach contents of collected specimens. The composition of organohalogen compounds is determined in blubber samples, and assessment and mitigation of bycatch are conducted using observers onboard fishing vessels. Fisheries bycatch data showed that Indo-Pacific bottlenose dolphins occur year round in all areas around Zanzibar. Sexual maturity was attained between 7 and 8 years and body length 190-200 cm in females and at 16 years and body length 213 cm in males. The gestation period was estimated to be 12.3 months, with calving occurring throughout the year, peaking November-March and with an interval of 2.7 years. The estimated pregnancy rate was between 0.10 and 0.58 depending on methods used. Stomach contents revealed a relatively large number of prey species, but that only a few small- and medium-sized neritic fish and cephalopods contribute substantially to the diet. Estimates of total annual bycatch were >9% which is not considered sustainable. An experiment showed that pingers can be a short term mitigation measure to reduce bycatch of dolphins in both drift- and bottom set gillnets. Methoxylated polybrominated diphenyl ethers (Meo-BDEs) were found at higher concentrations than anthropogenic organic pesticides (OCPs), with only traces of polychlorinated biphenyls (PCBs) detected. This study reveals the magnitude and apparent susceptibility of Indo-Pacific bottlenose dolphins off Zanzibar to anthropogenic threats, especially fisheries bycatch, and it is clear that immediate conservation and management measures are needed to reduce bycatch. Keywords: Growth, reproduction, feeding ecology, bycatch, organohalogen compounds, dolphins, Tursiops aduncus, Zanzibar, East Africa.

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LIST OF PAPERS This thesis is based on the following papers, which are referred to in the text by their roman numerals

I Amir, O.A., Jiddawi, N.S. & Berggren, P. (2005). The occurrence

and distribution of dolphins in Zanzibar, Tanzania, with comments

on the differences between two species of Tursiops. Western Indian

Ocean Journal of Marine Sciences 4, 85-93.

II Amir, O.A., Berggren, P. & Jiddawi, N.S. Growth and reproduction

of Indo-Pacific bottlenose dolphins (Tursiops aduncus) incidentally

caught in gillnets off Zanzibar, Tanzania. Submitted to Marine

Biology.

III Amir, O.A., Berggren, P. Ndaro, S.G.M. & Jiddawi, N.S. (2005).

Feeding ecology of the Indo-Pacific bottlenose dolphin (Tursiops

aduncus) incidentally caught in the gillnet fisheries off Zanzibar,

Tanzania. Estuarine, Coastal and Shelf Science, 63: 429-437.

IV Amir, O.A. and Berggren, P. Estimates of bycatch and field

experiment using pingers to reduce bycatch of dolphins in drift- and

bottom set gillnets in Menai Bay, Zanzibar, Tanzania. Manuscript.

V Mwevura, H., Amir, O.A., Kishimba, M., Berggren, P. & Kylin, H.

Organohalogen compounds in blubber of Indo-Pacific bottlenose

dolphin (Tursiops aduncus) and spinner dolphin (Stenella

longirostris) from Zanzibar, Tanzania. Submitted to Environmental

Pollution.

Published papers are reprinted with kind permission from the publishers.

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TABLE OF CONTENTS INTRODUCTION .................................................................................... 1

Worldwide distribution of Indo-Pacific bottlenose dolphins ..................... 1

Population structure and abundance of Indo-Pacific bottlenose around

Zanzibar .................................................................................................. 2

Biology (life history) .............................................................................. 3

Ecology (feeding and diet) ...................................................................... 3

Anthropogenic threats of marine mammals ............................................. 4

Incidental catch (bycatch) in fisheries: assessment and mitigation

measures ............................................................................................ 4

Persistent organic pollutants (POP) effect on marine mammals ........... 6

Conservation and management ................................................................. 8

OBJECTIVES OF THE THESIS ............................................................ 8

MATERIALS AND STUDY AREAS ...................................................... 9

METHODS AND SUMMARIES OF THE PAPERS ............................... 9

RESULTS AND DISCUSSION .............................................................. 13

Occurrence and distribution .................................................................. 13

Growth and reproduction ...................................................................... 13

Feeding ecology and diet ....................................................................... 14

Assessment and mitigation of bycatch ................................................... 15

Organohalogen compounds ................................................................... 15

CONCLUDING REMARKS ................................................................. 16

REFERENCES ....................................................................................... 18

ACKNOWLEDGEMENTS ................................................................... 29

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INTRODUCTION A population may be defined as a group of organisms of the same species occupying a particular space at a particular time (Krebs 1994). However, the distribution of organisms is seldom random in space (Boyce & McDonald 1999). For instance, the distribution of marine mammals varies according to the physical, chemical and biological characteristics of the marine habitats they use (Forcada 2009). If habitats differ in quality, individuals should be expected to exhibit some degree of habitat selection, in order to take maximum advantage of available resources (Wiens 1976). Thus, the way organisms interact with their physical and biological environment not only determines their patterns of distribution and abundance, but has also fundamental effects on the dynamics, social structure, evolutionary trajectory and conservation of populations (Krebs 1994). Generally, the distribution of marine mammals can be classified as coastal (in estuarine or near-shore waters), neritic (in waters on the continental shelf) or oceanic (in waters beyond the continental slope, in the open seas or oceans), which can be found in tropical and/subtropical, temperate, Antarctic or Arctic waters (Forcada 2009).

Worldwide distribution of Indo-Pacific bottlenose dolphins Indo-Pacific bottlenose dolphins (Tursiops aduncus) have discontinuous distribution in coastal warm temperate to tropical marine waters of the Indo-Pacific region (Reeves & Brownell 2009; Wang & Yang 2009). They are found from the southern tip of Africa in the west, along the northern rim of the Indian Ocean (including the Red Sea, Arabian Gulf and Indo-Malay Archipelago to as far east as the Solomon Islands and New Caledonia) and western side of the Pacific to the southern half of Japan and the southern coast of Australia (Figure 1) (Wang & Yang 2009). The species has a limited coastal range throughout much of the Indo-Pacific Ocean except in areas with wide continental shelves (Reeves & Brownell 2009). Indo-Pacific bottlenose dolphins have also been confirmed to occur in near-shore waters of the east African region. Sighting records show that the species occurs along the coastal waters of Kenya (Wamukoya et al. 1996) and Mozambique (Berggren et al. 2007). Records of Indo-Pacific bottlenose dolphins in Tanzania are mainly from Zanzibar Island, which is located about 40 km from central Tanzania mainland coast. However, most of the survey efforts on distribution of dolphins have focused on Indo-Pacific bottlenose off the south coast of Zanzibar (e.g., Stensland et al. 1998; 2006). More surveys are required to better understand the distribution, population structure and

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abundance and ecology of small cetaceans in the entire waters of the east African region.

Figure 1. Distribution of the Indo-Pacific bottlenose dolphin (T. aduncus). Confirmed records are shown in blue and hypothesized distribution in olive. Question marks indicate uncertain records. The star indicates the geographical location where the holotype specimen was found (Source: Wang & Yang 2009).

Population structure and abundance of Indo-Pacific bottlenoses around Zanzibar Knowledge of the population structure is essential for a proper evaluation of the distribution and abundance of a species as well as to assess the impact of bycatches in any particular area. At least two populations of Indo-Pacific bottlenose dolphins have been reported to occur in Zanzibar coastal waters. Analyses of genetic differentiation in mitochondrial DNA suggest a significant separation between the Indo-Pacific bottlenose dolphins found off northern and southern coasts of Zanzibar (Särnblad et al. submitted). Abundance of this species has only been estimated for a few areas and most populations are thought to be small. For example, the size of the resident population off the south coast of Zanzibar has been estimated to 136 (95% CI 124-172) animals in 2002 based on mark-recapture analysis of photographically identified dolphins (Stensland et al. 2006). The year-round occurrence and social organization of this species off the south coast of Zanzibar suggest that this area may be important as a feeding and calving area (Stensland et al. 2006). Indo-Pacific bottlenose dolphins have been

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observed in association with spinner dolphins (Stenella longirostris) off the north coast (Ortland 1997) and with Indo-Pacific humpback dolphins (Sousa chinensis) off the south coast of Zanzibar (Stensland et al. 2006).

Biology (life history) The life history of a species describes how available resources are distributed between survival, growth and reproduction. In many marine mammals, particularly in cetaceans, this has resulted in life histories characterized by high survival (for both calf and adult), long life span, late reproductive maturity, a single offspring, relatively long gestation and nursing periods, and long inter-birth period. Data from life history studies are also imperative for assessment of non-natural mortalities e.g. directed fisheries, fisheries bycatch or contamination effect on marine mammal population viability (Hohn et al. 1996; Wells et al. 2005; Soykan et al. 2008; Murphy et al. 2009).

To understand the population dynamics of dolphins it is important to know the age and size at which animals reach sexual maturity and thus when the species initiates breeding (Bryden & Harrison 1986). It is important to note that the age and size at sexual maturity may differ significantly within a cetacean species due to several factors, such as climate, diet and exploitation (Bryden & Harrison 1986). To date, there is no information on the growth and reproductive biology of Indo-Pacific bottlenose dolphin populations found in the east African region.

Ecology (feeding and diet) The distribution of many marine mammals is related to that of their preferred prey (Gaskin 1982; Bowen et al. 2002; Ballance 2009; Forcada 2009). For example, seasonal abundance of common dolphins (Delphinus delphis) off the southeast coast of Africa closely parallels the annual sardine run (Young & Cockcroft 1994). Similarly, the winter distribution of killer whales (Orcinus orca) in Norwegian waters underwent major changes following the distributional shift in spring-spawning herring during the late 1980’s (Similää et al. 1996). Therefore, reliable information on diet composition and food habits contributes important information for understanding the distribution and abundance of small cetaceans.

Most of what is known about the food of marine mammal predators comes from data collected from dead animals, through directed fisheries, incidental mortality or strandings (Balance 2009). Analyses of their stomach contents can be useful for many other investigations, such as (i) understanding spatial and temporal distribution of predators; (ii) studies of

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predator-prey dynamics; (iii) the ecology of the prey species in the area available to predators; and (iv) changes in diet during growth and over time (Barros & Clarke 2009). An estimate of diet composition from analysis of stomach contents has some disadvantages since it depends on the diagnostics of hard part remains, mainly fish otoliths and cephalopod beaks. Such disadvantages include underrepresentation of prey with no hard parts and/or being less digestible. This can complicate the calculation of reconstructed meal sizes of prey with different digestion rates (Pierce & Boyle 1991; Pierce et al. 2007; Barros & Clarke 2009). However, analysis of stomach contents provides information at considerably less cost compared to other methods and samples can be collected from carcasses in an advanced stage of decomposition (Barros & Clarke 2009).

Marine mammals eat a great variety of animals from minute crustaceans (<1mm long) to giant squids (>15m long) (Barros & Clarke 2009). In toothed whales, the main prey items are fish and cephalopods, but the relative proportions and importance of the prey species depend on the predator species (Barros & Clarke 2009). For example, the diet of bottlenose dolphins caught in shark nets along the Natal coast of South Africa was dominated by fish and cephalopods accounting for 75% 25%, respectively of the prey mass (Cockcroft and Ross 1990b). Meynier et al. (2008) found that fish accounted for 94.4% by mass in the diet of the short-beaked common dolphin (Delphinus delphis) in the Bay of Biscay and 84.2% of the diet by number. Meanwhile, cephalopods, crustaceans and fish represented approximately 94%, 3% and 3% by number of prey items respectively in the diet of pygmy sperm whales (Kogia breviceps) stranded in New Zealand (Beatson 2007). Currently, no dietary study has been conducted on the Indo-Pacific bottlenose dolphins in east African region.

Anthropogenic threats of marine mammals Numerous anthropogenic activities have been identified as threats to marine mammal populations worldwide. They include, but not limited to, incidental catch (bycatch) in fisheries, pollution, tourism, acoustic disturbance and habitat degradation. The following section reviews the potential threats of bycatch and pollution relevant to this thesis for Indo-Pacific bottlenose dolphins in east Africa.

Incidental catch (bycatch) in fisheries: assessment and mitigation measures Bycatch of marine mammals is the unintended capture of marine mammals in fishing operations, in addition to the targeted species towards which fishing effort is directed (Northridge 2009). Bycatch is understood to be the

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major threat to the conservation of marine mammals, not only in east Africa, but also throughout the world’s oceans (Reeves et al. 2003; Read et al. 2006).

It is thought that nearly all small cetaceans have rates of population growth no higher than about 4% per year (Reilly & Barlow 1986; Wade 1998; Moore & Read 2008). Certainly, no dolphin population has been observed to increase at a faster rate, and aspects of their life history (late reproductive maturity, a single offspring, relatively long gestation and nursing periods, and long inter-birth period) make faster rates unlikely for dolphins (Reilly & Barlow 1986). The Scientific Committee (SC) of the International Whaling Commission (IWC) have agreed that annual anthropogenic mortalities >2% of best available abundance estimate may not be sustainable for the population concerned (IWC 1996). For example, it concluded that levels of directed takes exceeding 2% of the abundance of Dall’s porpoises (Phocoenoides dalli) are unlikely to be sustainable and recommended that such catch levels be reduced to sustainable levels as soon as possible (IWC 2002; 2006). In addition, it determined that a 1% removal level for a small coastal population of franciscana (Pontoporia blainvillei) in the western South Atlantic was sufficient to warrant concern about the status (IWC 2005).

The status of cetaceans can be evaluated by estimating the extent and magnitude of a given threat within the geographical area of concern as well as to develop an understanding of its effect on individual animals and populations (Whitehead et al. 2000). It has been recognized that incidental mortality in gillnet fisheries is the most important conservation problem in the east African region, including Zanzibar (Kiszka et al. 2008). The level of bycatch of dolphins in gillnet fisheries of Zanzibar have previously only been investigated in a questionnaire survey conducted in 1999 where a large number of bycatches was reported in the drift gillnet fishery (Amir et al. 2002). However, the total bycatch and its impact on dolphin populations off Zanzibar are not known. In order to estimate the total magnitude of bycatch of dolphins and to assess its impact on the populations concerned it is necessary to conduct a survey using independent observers onboard fishing vessels (Northridge & Thomas 2003).

There are many potential ways to solve a bycatch problem provided that the legal framework and the necessary resources are available. For example, particular areas or seasons where bycatch occur can be closed to a fishery. The fishing gear can be changed or modified to eliminate or reduce the bycatch. The animals can be scared away from the fishing gear with a noise-making device. However, the only method that is always successful in ending bycatch is to close the fishery, but this of course is a very extreme measure (Perrin et al. 2005). One potential alternative to reducing bycatch of small cetaceans in gillnets is to alert or deter the animals from the net acoustically. Pingers are low intensity underwater acoustic warning devices

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that emit a pulsed signal between 2.5 and 12 kHz (Stewardson & Cawthorn 2003). Some studies have shown that pingers can be effective in mitigating bycatch of some species of cetaceans (e.g., Kraus et al. 1997; Bordino et al. 2002; Barlow & Cameron 2003). When attached at regular intervals along the length of a net, pingers have been shown to reduce the numbers of bycaught marine mammals, including harbour porpoises, dolphins and sea lions (Northridge 2009). Although pingers have been found to reduce bycatch of some cetacean species in gillnets, their effect will not be equal for all species and in all situations (ICES 2002). Therefore, the effectiveness of pingers in reducing bycatch of dolphins in east Africa region need to be investigated since they have not been tried previously in the area.

Persistent organic pollutants (POP) effect on marine mammals The concept of pollution incorporates many different substances to which marine mammals are exposed and which may affect their health adversely. These include chemical compounds, oil derived substances, marine debris, sewage-related pathogens, excessive amounts of nutrients causing environmental changes and radio-nuclides (Reijnders et al. 2009). However, some substances are of specific concern and hence the subject of focused research on marine mammals has been placed upon organohalogenated compounds (Reijnders et al. 2009). The organic compounds comprise both chlorinated e.g., polychlorinated biphenyls (PCBs), dichlorodiphenyl-trichloroethane (DDT) and its metabolites, hexachlorobenzene (HCB) and hexachlorocyclohexanes (HCHs), dieldrin, endrin, mirex and brominated e.g., polybrominated diphenyl ethers (PBDEs) (Law 1996). PBDE flame retardants represent a more recent concern in marine mammals and as such have gained scientific interest (Reijnders et al. 2009). There is concern that this group of chemicals has the same characteristics as the UNEP short-listed POPs, being persistent, toxic, bioaccumulative and widely distributed throughout the environment. These compounds have emerged as a significant global concern for fish and marine mammals (Ross et al. 2009). Methoxylated (MeO) PBDEs are also known to accumulate in marine mammals from natural marine sources, such as algae (Malmvärn et al. 2005) and sponges (Agrawal & Bowden 2005). The POPs are globally distributed, reaching high levels in many marine mammals as a function of proximity to source and trophic level. In this way, while populations inhabiting industrialized areas are most vulnerable (Ross et al. 2004), even those in remote regions have become contaminated (Muir et al. 2000).

High trophic level marine mammals (fish- or marine mammal-eating species) are considered as particularly vulnerable to the magnification of persistent, bioaccumulative and toxic compounds including several members of the persistent organic pollutant (POP) family (Bennett et al. 2009). There are a number of specific biological reasons why marine mammals are

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amongst the wildlife most vulnerable to the long-term effects of hazardous man-made chemicals (Tanabe et al. 1994; Colborn & Smolen 1996). They are particularly susceptible to these pollutants because they store the chemicals in their blubber, which acts as a reserve for ingested lipophilic chemical contaminants (such as DDT and PCBs, Dioxin), have a limited capacity to metabolise these substances and pass them on to their young who often are the most vulnerable to the effects of chemicals. The effects of POPs and other contaminants on marine mammals are unclear, although POPs, and the PCBs in particular, have been found to have negative impact on populations in certain regions (Reijnders 1994; Jepson et al. 2005). For example, a high frequency of complex pathological disorders and reproductive impairments were described in Baltic grey (Halichoerus grypus) and ringed seals (Phoca hispida) during the 1960s and 1970s, when these seals were exposed to particularly high burdens of PCBs and DDTs (Helle et al. 1976; Bergmen and Olsson 1986; Olsson et al. 1994;). Furthermore, high burdens of PCBs have been associated with population declines in the European otter (Lutra lutra), including populations from the Baltic Sea (Sjöasen et al. 1997; Roos et al. 2001)

High tissue concentrations of some pollutants, including heavy metals, some persistent organochlorine compounds, including PCBs and pesticides (POPs) and emerging chemicals such as brominated flame retardants have been associated with organ anomalies, impaired reproduction and impaired immune function (Kannan et al. 2000; Schwacke et al. 2002). However, a clear cause and effect relationship between environmental contaminants and the observed effects has been demonstrated in only a few studies (Reijnders et al. 2009). Semi-field studies have demonstrated links between POP exposure (accumulation) and effects on the endocrine and immune systems of pinnipeds (Reijnders 1986; De Swart et al. 1996; Ross et al. 1996). Field studies of both pinnipeds and cetaceans have demonstrated correlations between tissue contaminant levels and various health ‘biomarkers’ in different species, providing speculative (i.e. not mechanistic) evidence of POP-related impacts (Subramanian et al. 1987; Jepson et al. 1999; Fossi et al. 2000; Simms et al. 2000; Nyman et al. 2003). Such evidence suggests that heavily contaminated populations may suffer from reproductive impairment, developmental abnormalities and increased susceptibility to disease, although confounding factors (e.g. age, sex, condition, etc) may play a role in some of these observations (Ross 2002; Ross et al. 1996; Reijnders et al. 2009). To date, nothing is known about the level of organic pollutants for Indo-Pacific bottlenose dolphins in the east African waters.

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Conservation and management Many people, including scientists, have become particularly concerned about the status of cetacean populations. This is because of their ecological significance, their economic value (both dead and alive), their potential as indicators of aquatic pollution and thus the view that cetaceans should be conserved prevails (Whitehead et al. 2000). The urgency of obtaining information on the status of cetaceans in the east African region has been acknowledged by the Scientific Committee of the IWC (Anonymous 1998). The status of Indo-Pacific bottlenose dolphin populations throughout most of east African region is poorly known. Reeves & Brownell (2009) have expressed the need to determine the conservation status of Indo-Pacific bottlenose dolphin populations especially around islands where human-caused mortality or removal (direct or incidental catch) is known to occur. Being restricted to the near-shore distribution along the coastal waters of the east African region, Indo-Pacific bottlenose dolphins are highly vulnerable to numerous existing anthropogenic threats.

At present, it is not possible to assess the population status of Indo-Pacific bottlenose dolphins in east African waters because information on their biology and ecology is limited. The sparse data available for selected areas indicate that Indo-Pacific bottlenose dolphins occur in discrete, geographically localized populations and are susceptible to anthropogenic threats (e.g., incidental captures in gill nets) (Amir et al. 2002). Information from this thesis together with information on abundance (Stensland et al. 2006), genetic population structure (Särnblad et al. submitted) and behaviour (Stensland and Berggren 2007; Christiansen et al. in press) provide the data necessary for the assessment of the overall impact of anthropogenic threats that Indo-Pacific bottlenose dolphin populations face and for conservation and management of the species in Zanzibar (Tanzania). Precautionary measures should be adopted while further work on abundance estimates, population structure, and levels of human-caused mortality need to be carried out on a wider scale in east African waters.

OBJECTIVES OF THE THESIS The overall objective of this thesis was to investigate the biology, ecology and anthropogenic threats of Indo-Pacific bottlenose dolphins off Zanzibar, Tanzania, east Africa. Specifically, the objectives were to; investigate the occurrence and distribution (Paper I), describe growth and reproduction (Paper II) examine feeding ecology and diet (Paper III) estimate and assess impact of bycatch in gillnet fisheries as well as investigate the effectiveness of pingers as a potential mitigation measure for reducing the bycatch (Paper IV) and describe accumulation and composition of organohalogen compounds (Paper V).

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MATERIALS AND STUDY AREAS Specimens used in the studies were collected from gillnet fisheries bycatch between 2000 and 2008 off Zanzibar (Figure 2). Biological samples and physical data were collected during dissections performed at the Institute of Marine Sciences (IMS), Zanzibar. Prior to dissection, the total body length was measured to the nearest centimetre in a straight line from the tip of the upper jaw to the fluke notch and the weight was recorded to the nearest kilogram. Sex of the specimens were determined externally and confirmed by examination of gonads. Field studies using observer programmes on drift- and bottom set gillnet fisheries were carried out in the Menai Bay Conservation Area (MBCA), on the southwest coast of Zanzibar (Figure 2).

METHODS AND SUMMARY OF PAPERS

Occurrence and distribution (Paper I) In the first paper, we describe the occurrence and distribution of different species of dolphins around Zanzibar. This was done by examining records of 143 dolphins reported as incidental catch by fishermen from 12 fish landing sites around Zanzibar between 2000 and 2004. In this paper we also suggest that the large number of incidental catch of dolphins recorded in gillnet fisheries indicate that bycatch may be a potential threat to local populations that need to be addressed in future conservation and management efforts in the region.

Growth and reproduction (Paper II) In the second paper, growth and reproduction of Indo-Pacific bottlenose dolphins were investigated using teeth, ovaries and testes recovered from 69 incidental caught specimens between 2000 and 2008. Age was estimated by counting annual growth layer groups (GLGs) in decalcified and stained sections of teeth following the recommendations by Perrin & Myrick (1980). The sexual maturity of animals was determined by gonadal examination. Sexual maturity in females was determined from evidence of ovulation (presence of at least one corpus luteum, CL or corpus albicans, CA) on either ovary following Perrin & Donovan (1984), unless the female was obviously sexually mature at the time of capture (i.e., pregnant or lactating).

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Figure 2. Map showing location of Zanzibar and the Menai Bay Conservation Area.

For males a combination of histological examination and weight of the testis were used in the determination of sexual maturity (Collet & Saint Girons 1984). The growth of the animals was investigated using age and length measurements recorded during full autopsies. Both the reproductive and

Menai Bay Conservation

Area

Kizimkazi

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growth data were combined with the age analyses to provide sex specific estimates of maturity, reproduction and growth of Indo-Pacific bottlenose dolphins off Zanzibar.

Feeding ecology and diet (Paper III) In the third paper, stomach contents from 26 specimens incidentally caught in gillnet fisheries between 2000 and 2002 were used to examine the foraging ecology and diet of Indo-Pacific bottlenose dolphins off Zanzibar. Specifically, this paper describes prey species composition, important prey species in the diet and comparison of diet between sex and maturity classes. Undigested prey were sorted, identified and measured (length and weight) when possible. Fish otoliths were identified using a published guide (Smale et al. 1995) and whole fish according to Smith & Heemstra (1986). Cephalopod beaks were identified using a reference collection from specimens bought in the local fish market. Four different indices were used to investigate the occurrence and relative importance of the prey found in the stomachs; percentage by number (% N), percentage frequency of occurrence (% FO), percentage by weight (% W) and an index of relative importance (IRI) (Pinkas et al. 1971).

Assessment and mitigation of bycatch (Paper IV) The fourth paper describes two observer programmes used to estimate and assess the impact of bycatch and to investigate the effectiveness of pingers in reducing the bycatch of dolphins in Menai Bay, Zanzibar. Specifically, in the first observer programme, the aim was to estimate the level of bycatch in gillnet fisheries and to assess the impact on populations of Indo-Pacific bottlenose and humpback (Sousa chinensis) dolphins. This programme was conducted during 2003/2004 fishing season. Four onboard observers were randomly placed on 14 drift gillnet vessels and two observers were used to monitor 21 bottom set gillnet fishermen. The observers covered 23.6 % (372 km net*hours fished) of the total fishing effort of the drift gillnet fishery and 24.5% (1656 km net*hours fished) of the total fishing effort in bottom set gillnet fishery. To assess the impact of the bycatch, total bycatch was estimated for respective fishery and compared to the latest (2002) available population size estimates for respective species in Menai Bay.

In the second observer programme, the aim of the experiment was to evaluate the effectiveness of pingers in reducing bycatch of dolphins in gillnets as well as the impact of pingers on fish catches. This programme was conducted during 2007/2008 fishing season. In this programme, eight

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onboard observers were randomly placed on 21 drift gillnet vessels and two observers were used to monitor 26 bottom set gillnet fishermen. The observers collected data on fishery practice, date, time of departure and arrival, net soak time, number of panels set, fish catch and bycatch of dolphins. The observers were also involved in attaching and removing pingers. The observed effort in the drift gillnets was 257 control sets without pingers and 251 sets with pingers, 21% and 20% respectively of the total recorded effort. In the bottom set gillnet fishery, the observed fishing effort was 236 sets without pingers and 224 sets with pingers, 28% and 27% respectively of the total recorded effort.

Organohalogen compounds (Paper V) In the fifth paper, blubber samples were used to determine the accumulation and composition of organohalogen compounds in dolphins. The samples used were collected from 18 Indo-Pacific bottlenose and 18 spinner (Stenella longirostris) dolphins incidentally caught in gillnets between 2000 and 2002. The study also investigated sex and maturity-related differences within species and maternal transfer of quantified organohalogens was estimated for Indo-Pacific bottlenose dolphins. Blubber samples were taken from the left side in front of the dorsal fin, wrapped in aluminium foil, put into polythene bags and frozen at -20 °C until analysis.

Organohalogen compounds in blubber tissue were determined by ultra-trace congener-specific analysis, following methodology of Åkerblom (1995). This involved extraction and clean-up procedures. These principally included, Accelerated Solvent Extraction (ASE), purification by DCM/H2O and H2SO4/H2O partitioning, absorbent column chromatography, fractioning into coplanar and non-coplanar congeners and separate analysis. Organochlorine pesticides (OCPs) were quantified with gas chromatography equipped with two electron capture detectors (GC-ECD) on an Agilent 6890 (Agilent, Wilmington, Delaware, USA). Brominated compounds were identified by gas chromatography with electron capture negative ion mass spectrometry (GC-ECNIMS) ionization in the full scan mode. Mass spectra and retention times were compared with the spectra of MeO-BDEs reference standards that were kindly provided by Åke Bergman, Environmental Chemistry Department, Stockholm University.

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RESULTS AND DISCUSSION

Occurrence and distribution (Paper I) The results from this study showed that at least six species of dolphins: Indo-Pacific bottlenose, common bottlenose (T. truncatus), spinner, pan-tropical spotted (S. attenuata), Risso’s (Grampus griseus) and Indo-Pacific humpback occur in waters around Zanzibar (Table 1 in Paper I). The majority of the dolphins were reported from the north coast. Two of the species (pan-tropical spotted and common bottlenose dolphins) have not previously been reported in the area. The data provide the first information on the geographical and temporal distribution of dolphin species around Zanzibar and thus help fill the gap in information of small cetaceans in East African coastal waters. Only one previously-reported dolphin species (Steno bredanensis) for the area was not represented in the samples. The larger number of dolphins caught in coastal waters north of Unguja Island likely reflects the greater fishing effort in this area (see, Amir et al. 2002). However, a broad survey of dolphin abundance would be necessary to confirm this.

Indo-Pacific bottlenose dolphins were the most common species identified, accounting for 48% of the total bycatch collected during the survey. The high percentage of Indo-Pacific bottlenose dolphins caught in gillnets in the coastal waters indicates that they may be the most abundant inshore dolphin species around Zanzibar. This is also supported by the high percentage of this species in a previous survey of the incidental catch of dolphins in the gillnet fisheries in Zanzibar (Amir et al. 2002). Further, Indo-Pacific bottlenose dolphins share coastal habitats with Indo-Pacific humpack dolphins off the south coast of Unguja Island (Stensland et al. 1998; 2006), and with spinner dolphins off the north coast by Nungwi and Matemwe (Ortland 1997). Preliminary results from genetic analyses using mitochondrial DNA, from specimens collected from bycatch and animals sampled in the field, indicate a restricted gene flow and limited female dispersion between northern and southern Zanzibar (Särnblad et al. submitted).

Growth and reproduction (Paper II) The results from this study suggest that sexual maturity in females is attained between 7 and 8 years (Fig. 5 in Paper II) at a total body length between 190 and 200 cm (Fig. 6 in Paper II). Onset of sexual maturity of male Indo-Pacific bottlenose dolphins may be attained at about 16 years (Fig. 8 in Paper II) and at a total body length of 213 cm (Fig. 9 in Paper II). The

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gestation period was estimated to be 12.3 months, with calving occurring throughout the year, peaking November-March and with an interval of 2.7 years. The estimated pregnancy rate was between 0.10 and 0.58 depending on methods used.

The predicted asymptotic body length for female dolphins was 222.3 cm (Fig. 3a in Paper II) and for male dolphins was 223.4 cm (Fig. 3b in Paper II). There was no significant difference in body length between adult male and adult female dolphins after the attainment of sexual maturity. The predicted asymptotic weight for females was 133.4 kg (Fig. 4a in Paper II) and for males was 150.2 kg (Fig. 4b in Paper II). Adult mature male were significantly heavier (mean = 151.1 kg, 95% CI = 137.2 to 165.1 kg) than adult mature female (mean = 125.9 kg, 95% CI = 119.42 to 132.4 kg) dolphins. Both the Gompertz growth model calculations (males =150.2 kg and females = 133.4 kg) and maximum weight (males =162 kg and females = 149 kg) in this study showed that there is sexual dimorphism in weight with males being significantly heavier than females. Cockcroft & Ross (1990a) also reported similar results for bottlenose dolphins from the east coast of southern Africa, which indicated sexual dimorphism in weight (males = 176 kg and females = 160 kg) but not in length.

Feeding ecology and diet (Paper III) A total of 1403 prey items comprising 50 species of bony fish and three species of squid were recorded in the stomach contents of the Indo-Pacific bottlenose dolphins investigated (Table 1 in Paper III). Fish were numerically the most important prey group (87% prey numbers), occurring in 92.3% of the stomachs. Cephalopods comprised 13% by number of the prey taken and were found in 50% of the stomachs that contained prey items. Fish were also the most important prey group by weight, constituting 83.5% of the mass of all prey consumed. The results showed that bony fishes were the most important food items for the Indo-Pacific bottlenose dolphins from waters around Zanzibar. These results support findings from previous investigations in other geographical areas which have reported that fishes are the most important food source of this species (Cockcroft & Ross, 1990b).

Although the diets comprised of a diverse range of fish and cephalopod species, the most important prey species included Uroconger lepturus, Synaphobranchus kaupii, Apogon apogonides, Sepioteuthis lessoniana, Lethrinus crocineus, Sepia latimanus, Loligo duvauceli and Lutjanus fulvus. These eight species contributed about 64.8% of the measured total weight of prey. The eight most important prey species also had the highest percentage number, percentage frequency of occurrence and percentage weight. The results agree with previous findings that only few prey species form the basis of the diet of Indo-Pacific bottlenose dolphins (Cockcroft & Ross 1990b).

Prey differences were evident between mature and immature animals, where Uroconger lepturus was the most important prey in mature dolphins

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whereas Apogon apogonides was the preferred prey of immature dolphins (Tables 2 and 3 in Paper III).

Assessment and mitigation of bycatch (Paper IV) During the observer programme in 2003/2004 three Indo-Pacific bottlenose dolphins were observed bycaught in drift gillnets and one Indo-Pacific humpback dolphin was observed bycaught in bottom-set gillnets. The bycatch rate for Indo-Pacific bottlenose dolphins in the drift gillnets was 0.0080 dolphins/km net*hours fished and the rate for Indo-Pacific humpback dolphins in the bottom set gillnet was 0.0006 dolphins/ km net*hours fished. The estimates of the total bycatch in the 2003/2004 fishing season were 13 Indo-Pacific bottlenose dolphins in the drift gillnet fishery and 4 humpback dolphins in the bottom-set gillnet fishery. To evaluate the biological significance of the documented bycatch in the study area, the ratios were calculated between the estimated bycatch in 2003/2004 and the latest (2002) population size estimate 136 (95% C.I. 124–172) Indo-Pacific bottlenose and 63 (95% C.I. 57-95) humpback dolphins in the study area (Stensland et al. 2006). The ratio 13/136 resulted in a 9.6 % removal rate of Indo-Pacific bottlenose dolphins in the drift gillnets and the ratio 4/63 resulted in a 6.3 % removal rate of humpback dolphins in the bottom set gillnets, during the 2003/2004 fishing season. These bycatch levels were not considered sustainable.

Six dolphins were bycaught during the pinger experiment in the drift gillnets (1 Indo-Pacific bottlenose dolphin in a net with pingers and 4 Indo-Pacific bottlenose dolphins and 1 spinner dolphin in the control nets without pingers) in 2007/2008 fishing season. In the bottom set gillnets, one humpback dolphin was bycaught in the control bottom set gillnet sets and no dolphin was bycaught in the bottom set gillnets sets equipped with pingers. Pingers reduced the bycatch of dolphins in both drift- and bottom set gillnets, however the reduction was only significant in the drift gillnets. Estimate of the total bycatch in the 2007/2008 fishing season were 16 Indo-Pacific bottlenose dolphins in drift gillnets and 3 humpback dolphins in the bottom-set gillnet fishery, representing 11.8% and 4.8% of estimated population size for respective species in the area in 2002. Given the documented unsustainable removal levels in the drift- and bottom set gillnets, immediate management actions are needed to reduce dolphin bycatch in these fisheries.

Organohalogen compounds (Paper V) Organochlorine pesticides (OCPs), brominated compounds and polychlorinated biphenyls (PCBs) were identified in the blubber of both

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Indo-Pacific bottlenose and spinner dolphins. The organochlorine pesticides identified included hexachlorobenzene (HCB), hexachlorocyclohexanes (HCHs), dichlorodiphenyltrichloroethane (DDT) and its metabolites DDE and DDD, the DDT analogue methoxychlor, and the cyclodienes aldrin, dieldrin, heptachlor, heptachlorepoxide and γ-chlordane. Essentially all of the anthropogenic compounds detected at quantifiable concentrations were pesticides, while only traces of compounds with industrial or other uses, such as polychlorinated biphenyls were found.

In addition to OCPs, both dolphin species contained MeO-BDEs, most likely of biogenic origin. Although the results indicated the presence of several brominated compounds, only two, 2′-methoxy-2,3′,4,5′-tetrabromodiphenyl ether (2′-MeO-BDE68) and 6-methoxy-2,2’,4,4’-tetrabromodiphenyl ether (6-MeO-BDE47) were confirmed and quantified as the authentic standards for other brominated compounds had not been accessed. The levels of OCPs measured in this study were lower than those reported in dolphins from other regions while MeO-BDEs were higher. The relative composition of the OCPs indicated recent use of lindane (γ-hexachlorocyclohexane, γ-HCH) and aged residues of the DDT group and technical HCH.

CONCLUDING REMARKS The research results presented in this thesis provide the first information

on the biology, ecology and anthropogenic threats of Indo-Pacific bottlenose dolphins off Zanzibar and indeed for the east African region. In addition to presenting better knowledge about the life history of a species which is poorly understood, this thesis contributes important information valuable to conservation and management of Indo-Pacific bottlenose dolphins in the region. The findings in the thesis demonstrate that Indo-Pacific bottlenose dolphins off Zanzibar inhabit near-shore waters and further that these areas constitute breeding and foraging grounds for the species. This conclusion is corroborated by the results from the stomach content analysis and the presence of lactating females and nursing calves in the bycatch.

The biological data of Indo-Pacific bottlenose dolphins off Zanzibar presented in the thesis, including age at sexual maturity (females 7-8 and males 16 years of age) and the average calving interval of about 2.7 years, conform to the life history characteristics of a long-lived mammal species with low fecundity, slow population growth rates and relatively late attainment of sexual maturity. Therefore, high incidences of incidental catch in gillnets will likely have negative impact on the growth of Indo-Pacific bottlenose dolphin populations off Zanzibar.

17

The data on the diet of the Indo-Pacific bottlenose dolphins presented in this thesis are also important in relation to current and future interactions with gillnet fisheries in the area. The stomach content analysis conducted suggests that Indo-Pacific bottlenose dolphins off Zanzibar are primarily piscivores, consuming a large amount of eel fish, and only a small proportion of cephalopods. The ecology and behaviour of the preferred fish prey species indicate that the dolphins forage individually near shore, over reef or soft bottom substrates. Apparently, there is no significant threat to the food base of this species in Zanzibar waters, because the main components of their diet are not of commercial importance. However, due to the overlap between the dolphins’ foraging areas and the distribution of the gillnet fisheries (targeting species e.g., king fish, Scomberomorus commerson; tuna, Thunnus albacores and sailfish, Istiophorus platypterus), the foraging dolphins are threatened by incidental capture in the gillnets.

The results of this thesis have demonstrated that the mortality levels of Indo-Pacific bottlenose and humpback dolphins in Menai Bay are unsustainable. Hence, the demonstrated increase in gillnet fishing effort should be recognized as a threat to the long-term survival of Indo-Pacific bottlenose and humpback dolphins present in Menai Bay Conservation Area. Bycatch mitigation is important not only to conserve the dolphin populations, but also to protect the interests of local communities for which dolphin tourism has become an important source of their livelihood (Berggren et al. 2007). The result of the pinger experiment showed that pingers represent a short term mitigation measure to reduce bycatch of dolphins in both drift- and bottom set gillnets in Menai Bay. Therefore, pingers can be implemented while low cost long term measures are developed.

Currently, there are no published or universally acknowledged concentration thresholds for marine mammals by which to gauge the potential effects of organohalogen compounds (Meng et al. 2009). Therefore, the effect of organohalogen compounds recorded in this study on the general health of the two dolphin species remains unclear. However, it has been suggested that high concentrations of organohalogen compounds can have reproductive and/or health impact. For example, Sonne et al. (2005) suggested that the histologic changes in liver from east Greenland polar bears (Ursus maritimus) were a result of aging and long-term exposure to anthropogenic organohalogen compounds (OHCs). As the dominating organohalogens were presumably of natural origin, further studies to clarify local or regional sources, pathways for biomagnification and ecological consequences of natural organohalogen compounds in the region is needed.

In conclusion, the findings presented in this thesis on the biology, ecology and anthropogenic threats of Indo-Pacific bottlenose dolphins off Zanzibar demonstrate the need for immediate conservation and management measures to reduce dolphin bycatch. The experiment using pingers shows that this

18

provides one potential mitigation method that could solve the dolphin bycatch problem off Zanzibar and elsewhere in east Africa, at least in the short-term.

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ACKNOWLEDGEMENTS Many thanks and praises to Almighty God, who gives us guidance and appeals to our reasoning, so that we should use our intellect to understand and appreciate the marvels of His creation. Many people helped me over the past years; I owe a huge debt to all those who were kind enough to devote their time to this work.

First and far most, I would like to express a special appreciation to my main supervisor, Dr. Per Berggren for offering me this opportunity to carry out this work and for endless support and guidance and entrusting me in the project. Without his support, enthusiasm, useful criticism, constructive suggestions, corrections, discussions and to a great extent his close supervision on my work this thesis could not have been fulfilled. Since my beginning as an MSc student back in 2000, I have learnt a lot about dolphins, much that I was given the name “Omar Dolphin”. Many thanks should also go to my co-supervisors, Prof. Anders Angerbjörn at the Department of Zoology, Stockholm University for sharing his ideas about animal ecology and Dr. Narriman Jiddawi at the Institute of Marine Sciences, Zanzibar who introduced me to Dr. Per and being the first student from Tanzania to undertake study on marine mammals. Dr. Narriman has been willing to let me learn from her personal experience that has allowed my personal and academic growth as a researcher. Particular thanks are extended to my thesis committee, including Profs. Anders Angerbjörn, Bertil Borg and Hans Temrin, for their support and constructive criticisms of the research contained herein. They were of immense help during the write up of this thesis and their comments were invaluable.

I wish to express great thank to my dolphin (pomboo) colleagues Eva Stensland and Anna Särnblad of the Department of Zoology, Stockholm

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University and Khalifa Zam and his wife Saadiye of Kilimanjaro Club for their company and being part of my family in Sweden. They have been so kind to me beyond my expectations. Ylva Lillemarck from Museum of Natural History, Stockholm and Maria Bodin from the Department of Zoology, Stockholm are acknowledged for their help in various aspects of preparing of tooth sections and reading the age. I am indebted to wonderful people at Stockholm University; Prof. Sören Nylin, Prof. Tommy Radesäter, Anette Lorents, Berit Strand, Minna Miettinen and Ulf Norberg, who provided many helping hands and friendly favours with regard to administrative and technical issues. Many thanks should go to my roommates Augustine Mwandya, Dan Wilhelmsson and Saleh Yahya for providing a friendly, fun working environment and many stimulating discussions in our room. My appreciation is also expressed to previous and present PhD students, (Carlos, Ullasa, Ian, Marina, Magne, Jessica, Aleksandra, Mathias, Thomas and Karin) at the Department of Zoology, Stockholm University, for their cooperation and being so nice to me all the time. Thanks Mamboya, Kangwe, Sware and Mariam of the Department of Botany, Stockholm University for your company at different moment in Sweden.

I extend my sincere thanks to the Institute of Marine Sciences (IMS) for the fine logistical support and other assistance. Special thanks to Prof. Alfonce Dubi, the former Director of IMS, Dr. Marten Mtolera, coordinator of Sida/Sarec Bilateral Project, account section, typing pool, IMS dispensary, and numerous other staff at IMS who facilitated our project in many ways. It is impossible to conduct any field studies of cetaceans without the help of a dedicated team of helpers. For this I am particularly grateful to Salum Hamed, Mtumwa Mwadini, Dotto Salum, Ali Mwinyi, Kombo Ali, Idd Khamis and Muhiddin Abdalla of IMS, Zanzibar who helped out with unpleasant job of collecting specimens and dissections and Khaiyat Said for preparing chemicals. Thanks to my fellow students at IMS for your valuable support, good ideas and courage during my study.

I am extremely grateful to my employer, the Ministry of Agriculture, Livestock and Environment for allowing me to continue with the PhD study. The Department of Fisheries and Marine Resources of Zanzibar is acknowledged for granting me permission to carry out researches on dolphins and for providing field assistance through fish landing beach recorders. It is a pleasure to express my gratitude to all fishermen who submitted information on dolphins and specimens from incidental catches. Mr. Muhiddin Karabai from the Zanzibar Central Market provided assistance of collecting dolphins from the fishermen.

Several people in the scientific community, outside the department, have contributed to the success of this thesis. Thank you, Dr. Vic Cockcroft and Dr. Norbert Klages for kindly inviting me to come down south to Port Elizabeth Museum in South Africa and showing me how to identify prey items from stomach contents. Thank you, Dr. Christina Lockyer, of Age

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Dynamics, for accepting my request to come up to Tromso, Norway to learn about age determination of marine mammals and for your help in reading the age.

I would like to acknowledge the Stockholm University who funded my stay in Sweden for the last one and half years. The Swedish International Development Agency (SIDA) regional marine science programme administered by Swedmar and the WIOMSA through its MASMA programme are acknowledged for their financial support during the project.

Lastly, but not least, my sincerest thanks and best wishes to my family, for all they have done to get me this far. This thesis is dedicated to my parents, wife and children for their unwavering love, who bore the burden and not giving up but supporting me in every aspect during those PhD years.