OGONGO BERNARD OCHIENG THESIS.Pdf

SPECIES COMPOSITION, LENGTH-WEIGHT RELATIONSHIP AND

REPRODUCTIVE ACTIVITY OF EPINEPHELUS GROUPERS (PISCES:

SERRANIDAE) FROM SOUTH COAST KENYA INDIAN OCEAN WATERS

OGONGO, BERNARD OCHIENG’

A thesis submitted in partial fulfillment of the requirement of the Degree of Master of

Science in Fisheries of Pwani University

MARCH, 2015 ii

DECLARATIONS

iii

DEDICATION

This thesis is dedicated to my family, relatives, workmates and friends for their moral support, prayers, and encouragement throughout the study period.

ACKNOWLEDGEMENTS

The completion of this thesis could not have been possible without the direct support and contributions from my supervisors; Prof. Mwachiro Chenje Eric and Dr. Fulanda Mulwa

Bernerd who were always available and kept advising at every stage. Their guidance greatly contributed to the timely completion of the study. Indirectly, support and contributions came from Kenya Coastal Development Project (KCDP) through Kenya Marine & Fisheries

Research Institute (KMFRI) Programmes; Beach Management Unit (BMU) officials; fishery managers; the University; workmates (Boaz Orembo, Joseph Kilonzo and Sammy

Kadhenge); colleagues; wives (Sellina Atieno and Martha Asumo); children (Brian Ogongo,

Derrick Odhiambo, Flavian Achieng’ and Valentine Akinyi); brother (James Ogongo); and sisters (Everline Atieno and Anne Awuor) who provided excellent logistical work, connections, data collection assistance, dynamic challenging social and academic interaction learning environments. Thanks to all.

ABSTRACT

Globally, coastal and estuarine ecosystems are the most productive ecological systems providing essential ecosystem goods and services to the adjacent coastal populations. The ecosystems are however increasingly being threatened by anthropogenic activities leading to biodiversity loss and widespread impacts on important fishery species forming key pillars of many small-scale fisheries along the coast such as groupers. Epinephelus grouper species composition, LWR, and reproductive activity study was undertaken for eight (8) months beginning from December, 2013 from south coast Kenya Indian Ocean waters to provide data and information needed for supporting the fishery conservation management measures.

Samples were collected for 3 consecutive days in each month from the artisanal fishermen in Msambweni, Shimoni and Vanga where the fishery is well established. Underwater visual censuses (UVCs) were further conducted to validate the landed species occurrences.

Detailed searches were undertaken to determine the presence of the individual Epinephelus grouper species within ~10 and 2.5-m width bands on either sides of the set transect lines at the fishing grounds and encountered individuals identified to species level, enumerated and data recorded by the same observer to ensure consistency. Likewise, samples collected from the artisanal fishers were also sorted to species level, total length (TL, cm) and body weights

(BW, g) measured for use in species composition; LWRs; and reproductive activity determinations. The species gonado-somatic indices (GSI) and sex ratios were determined from sexed, dissected and measured gonad weight (GW, g) results. The study revealed existence of 30 Epinephelus grouper species with varied individual numbers in which E. fasciatus and E. undulosus were the most and least abundant respectively. The species had similar (p > 0.05) site distributions; allometric LWRs (p < 0.01; b < 3); female favoured sex ratios; and reproductive activities occurring throughout the year with peaks from April through July

TABLE OF CONTENTS DeclarationsDeclarations…………………………………………………………………….…………..ii ...... Error! Bookmark not defined. Dedication ...... iii Acknowledgements ...... iv Abstract ...... v Table of contents ...... vi List of figures ...... viii List of tables ...... ix List of abbreviations and acronyms ...... x

CHAPTER ONE ...... 1 1. Introduction ...... 1 Problem statement ...... 2 Justification of the study ...... 3 Aims and objectives of the study ...... 3 Hypotheses ...... 4

CHAPTER TWO ...... 5 2. Literature review ...... 5

CHAPTER THREE ...... 9 3. Materials and methods ...... 9 Description of the study sites ...... 9 Research design ...... 10 Field sampling ...... 11 Processing of the gonad samples ...... 12 Determination of species composition and abundance ...... 14 Determination of length-weight relationships (lwrs) ...... 14 Estimation of fulton condition factors ...... 14 Determination of gonadosomatic indices (gsi, %) ...... 15 Determination of reproductive activity of epinephelus species ...... 15 Data and statistical tests for significance ...... 15

CHAPTER FOUR ...... 16 4. Results...... 16

vii

Species composition and abundance ...... 16 Length-weight relationships (lwrs) analyses ...... 22 Reproductive activity of epinephelus groupers ...... 26

CHAPTER FIVE ...... 34 5. Discussion ...... 34 Species composition and abundance of epinephelus groupers ...... 34 Length-weight relationships ...... 36 Reproductive activity of epinephelus groupers ...... 37

CHAPTER SIX ...... 40 6. Conclusions and recommendations ...... 40 Conclusions...... 40 Recommendations ...... 40

7. REFERENCES ...... 41

viii

LIST OF FIGURES `Figure 1: A map of Kenya (Inset) showing the location of the study sites; Vanga, Shimoni and Msambweni in South Coast, Kenya ...... 9 Figure 2: Diagram illustrating the long-swim transects method used in the UVC of the Epinephelus groupers in south-coast Kenya ...... 11

Figure 3: Species composition and numerical abundance (nos.) based on landings from the small scale fisheries and underwater visual counts (UVCs) for Epinephelus grouper species in the Indian Ocean waters of south coast Kenya during the study ...... 17 Figure 4: Length-weight relationships’ for E. acanthistus, E. areolatus, E. bentoides, E. chlorostigma E. coeruleopunctatus, E. coioides, E. diacanthus, E. fasciatus, E. flavocaeruleus, and E. fuscoguttatus from the small-scale fisheries in south coast, Kenya ...... 23 Figure 5: Length-weight relationships’ for E. hexagonatus, E. lanceolatus E. longispinis, E. macrospilos, E. malabaricus, E. melanostigma, E. merra, and E. miliaris from the small-scale fisheries in south coast, Kenya ...... 24 Figure 6: Length-weight relationships’ for E. multinotatus, E. poecilonatus E. rivulatus, E. spilotoceps, and E. tauvina from the small-scale fisheries in south coast, Kenya ...... 25 Figure 7: Monthly maturity stages between female and male Epinephelus grouper species sampled during the study...... 30

LIST OF TABLES Table 1: Criteria used in the determination of maturity stages of grouper species in the present study ...... 13

Table 2: Number of landed specimens of Epinephelus groupers by species and site during the present survey in south coast Kenya ...... 19

Table 3: Variations in the numerical abundance of landed specimens for each specimen in NEM and SEM seasons during the present study ...... 21

Table 4: Sex ratios of Epinephelus grouper species from the small-scale fisheries of south coast Kenya ...... 27

Table 5: Monthly Fulton Condition Factor (KF) for species of the Epinephelus groupers landed by the small-scale marine fisheries in South-coast Kenya ...... 32

LIST OF ABBREVIATIONS AND ACRONYMS

BMU Beach Management Unit

CBD Convention on Biological Diversity

CITES Convention on International Trade in Endangered Species

FAO Food and Agriculture Organization of the United Nations

GoK Government of Kenya

GPS Global Positioning System

GSI Gonado-somatic Index

KCDP Kenya Coastal Development Project

KMFRI Kenya Marine and Fisheries Research Institute

KF Fulton Condition Factor

LWR Length-Weight Relationship

MEA Millennium Ecosystem Assessment

NEM North east monsoon

SEM South east monsoon

SPAGG Spawning Aggregations

SDF State Department of Fisheries

TL Total length

UNEP United Nations Environmental Programme

IUCN International Union for Conservation of Nature

UVC / UVS Underwater Visual Census (Survey)

WIO Western Indian Ocean

WIOMSA Western Indian Ocean Marine Science Association

CHAPTER ONE

1. INTRODUCTION

Groupers or rock cods are teleost fishes belonging to the family Serranidae in the order

Perciformes. The family contains more than 400 species and is widely distributed in tropical and sub-tropical seas all over the world (Heemstra & Randall, 1993). The term “grouper” usually refers to the serranid fishes in the sub-family Epinephelinae which is comprised of about 15 genera with 159 species (Sattar et al. , 2012). The Epinephelus genus comprises 98 species (Heemstra & Randall, 1993) and is an important component of the inshore small- scale fisheries along the Eastern coast of Africa where they are locally known as “Tewa”

(Anam & Mostarda, 2012). Majority of the species are typically stout and compressed, with slightly elongate bodies covered with brown spots or blotches (Plate 1).

Plate 1: Typical body forms of Epinephelus groupers

The Epinephelus species are mostly demersal (benthic or bottom-oriented) solitary predatory fishes inhabiting shallow coastal waters of less than 200 m depth (Bullock & Smith, 1991) preferring coral reef habitats and rocky substrates. The species are generally large sized compared to other species of the small-scale reef fisheries with some species attaining sizes over 1-m long and body weights of up to 100 kg. In addition, the species generally have very large mouths and protruding lower jaws making them slow swimmers (Bullock & Smith,

1991). Most members of the genus are sedentary, long-lived, and slow to mature with some attaining sexual maturity only after 8 to 10 years. Groupers are widely distributed in the marine waters of Eastern Africa, Indo-west Pacific, Red Sea, Philippines, Southern Japan and

Hawaii and support rich commercial and small-scale fisheries within these coasts (Aguilar-

Pereira, 2006).

Although little attention has been given to the study of the reproductive biology of most of these species, it appears that majority of the members are likely protogynous hermaphrodites, maturing first as females, and changing sex to male after the first or second spawn (Avise &

Mank, 2008). Further, majority of the species are characterized by spawning aggregations that are highly predictable in time and space, thus making the groupers highly vulnerable to growth over-fishing where many are caught before attaining sexual maturity (Johannes et al. ,

1999; Rhodes & Tupper, 2007).

Problem statement

Globally, marine biodiversity is under increasing threat due to numerous factors including overfishing, climate change, pollution and habitat destruction among others (Pullin et al. ,

2004; WWF, 2006). Fishes have particularly been more vulnerable to these threats due to changing fishing patterns, illegal, unreported and unregulated (IUU) fishing, poor fisheries management, and use of deleterious fishing gears and techniques that negatively impact on

fish stocks and the environment (Sattar et al. , 2012). The result has been a huge decline in fish stock calling for increased conservation efforts by governments and conservation managers as well as development of multilateral agreements and conservation action strategies guided by scientific research and high quality science. Examples of such strategic efforts include the Convention on Biological Diversity (CBD) and the Convention on

International Trade in Endangered Species (CITES) (Millennium Ecosystem Assessment-

MA, 2005; Pauly et al ., 2005).

Justification of the Study

The Epinephelus groupers are among the most common serranid reef fishes in the small scale coastal and marine fisheries and in Kenya they comprise important sources of food and income to the coastal communities (Ochiewo, 2004). However, the Epinephelus fisheries have reportedly been on the decline forcing fishers to wander far and wide in search of richer fishing grounds for these fishes (Bini et al. , 2005; Agembe et al. , 2010). Consequently, a clearer understanding of the biology and population dynamics of these species, and especially with reference to species composition, length-weight relationships and reproductive activities is not only of general ecological importance, but also critical to the sustainable exploitation of these important fisheries (Bellwood et al. , 2004). The present study was therefore aimed at providing this crucial species-specific data information for the Epinephelus groupers along the Kenya coasts to aid the formulation of management interventions for sustainable utilization of these important fisheries and curb the reported decline in fish stocks (Kaunda-

Arara et al. , 2003; Agembe et al. , 2010).

Aims and objectives of the Study

The overall aim this study was to study the biology of the Epinephelus grouper species and the determine species composition, abundance, length-weight relationship and reproductive

activity based on samples from the small scale fisheries of Kenya ’s south coast Indian Ocean waters and to provide the much needed information for the management of grouper fisheries.

Specifically, the objectives of the study was to;-

i) Determine the species composition and abundance of the Epinephelus groupers in the

small-scale fisheries along south coast of Kenya.

ii) Determine and describe the length-weight relationships’ (LWRs) of the landed

grouper species.

iii) Describe the reproductive activity the Epinephelus groupers from selected study sites

along the south coast of Kenya.

Hypotheses

The hypotheses for the study were that;-

H0: There are no significant differences in species composition, abundance, length-weight

relationships’ and reproductive activity of Epinephelus groupers from different fishing

grounds along the south coast Indian Ocean waters of Kenya.

HA: There are significant differences in species composition, abundance, length-weight

relationships’ and reproductive activity of Epinephelus groupers from different fishing

grounds along the south coast Indian Ocean waters of Kenya.

CHAPTER TWO

2. LITERATURE REVIEW

Globally, the Epinephelus groupers represent very important species as economic and ecological components of small-scale reef fisheries of the tropical and subtropical seas and many of these species are highly valued for food (McClanahan & Graham, 2005; Agembe et al. , 2010). Due to the typical multi-gear nature of the small-scale reef fisheries, majority of the species are landed as both target species or as by-catch thus driving the reported declines recorded in many of the grouper fisheries along many coasts (Chan et al. , 2007; Gillet &

Moy, 2006; Agembe et al. , 2010; Colin, 2012). Many of the grouper species are also reported as hermaphroditic with resultant lower levels of fertilization and higher probability of unfertilized egg batches especially when many of the males of the same cohorts are much smaller males than the females during a certain spawning season (Dulvy et al. , 2004;

Munday et al ., 2006; Bostford et al. , 2007).

Decline in the Indo-Pacific grouper stocks has been well elaborated by studies of some

Epinephelus species within the Indian Ocean region (Esseen & Richmond, 2011) and in recent presentation at the United Nations Environmental Programme Convention in Nairobi

Kenya in 2015. Despite these reports, the Epinephelus species are still among the most targeted fishers in the small scale fisheries as sources of food and income partly due to their high market demand and premium prices, especially in the sushi and sashimi markets of

Southeast Asia (Rhodes & Tupper, 2007; Agembe et al. , 2010).The declines have further been augmented by ecological and environmental degradation of the natural habitats within the region which have further accelerated the decline in the abundance of the Epinephelus stocks (Campbell & Perdede, 2006; Bostford et al. , 2007; Esseen & Richmond, 2011).

Therefore, a better understanding of the biology of the grouper species of the reef fisheries

of south-coast Kenya is important for strategic management, sustainable exploitation, and conservation of the grouper stocks (Agembe et al. , 2010; Gupta et al. , 2011).

Length-Weight relationship (LWR) and Fish Condition factor are important parameters in the assessment of fish growth and body condition or well-being (Hossain et al. , 2011;

Hossain et al. , 2012; Rahman et al. , 2012). Therefore, LWRs and FCFs present important tools in fisheries biology and stock assessment studies worldwide (Bolarinwa & Popoola,

2013; Sarkar et al. , 2013). The length-weight relationship and body condition of fish is influenced by several factors including habitat and food availability, season, stomach fullness, sex, sexual and gonadal maturity and variations between species among others

(Sarkar et al. , 2013). Length-weight relationships also provide important clues on environmental and human interventions (Muchlisin et al. , 2010; Bolarinwa & Popoola,

2013; Sarkar et al. , 2013). For example, in stress free environments, most of the species report positive allometric growth (b>3) indicating a faster gain in weight than length

(Prasad & Anvar, 2007). However, it is also possible for shape to change even when b = 3 as a result to changes in the regression intercept “a” which may vary daily (Anderson &

Gutreuter, 1983; Cone, 1989).

Majority of fishes exhibit unisexualism or gonochory. They are therefore either born as males or females and remain so throughout their life (Wootton, 1991; Helfman et al ., 1997).

However, some species including the groupers exhibit varied sexual patterns including hermaphroditism; where the fish has either sexes (Mitcheson & Liu, 2008), simultaneous hermaphroditism where both sexes are active at the same time, or sequential hermaphroditism where the species inter-change sexes at some stage of its life. Sequential hermaphroditism can further divided into protogyny - in which the fish functions first as a female and later as male, or protandry - where the fish functions as a male first and later as female (Sadovy & Shapiro, 1987). This type of protogynous hermaphroditism is widely

found among many of the studied groupers in the Epinephelinae sub-family (Shapiro, 1987;

Rasotto & Shapiro, 1992; Mitcheson & Liu, 2008). Hermaphroditic or sex-changing fishes are reportedly more susceptible to over-fishing than their gonochoristic counterpart(Levin &

Grimes, 2002) with fishing that targets the larger individuals potentially leading to growth overfishing by differentially reducing the number of members of the stock (Hawkins &

Roberts, 2003; Alonzo & Mangel, 2004). In cases where the larger members are males, the result is often sperm limitations and resultant under fertilization during breeding (Parker,

1990; Coleman et al ., 1996). In some species, this is countered by “socially ” adjusting their sex ratios to reduce the limitation by alternating the overall male and female reproductive stocks (Mackie, 2003; Liu & Sadovy, 2004; Pandolfi et al. , 2009). A closer investigation of the reproductive activities of the small-scale reef and commercially exploited Epinephelus groupers is therefore important for assessment of their vulnerability for the design of appropriate management options (Rhodes & Sadovy, 2002). The importance of this information cannot be over-emphasized especially in the small-scale reef fisheries of south- coast Kenya where the grouper fisheries form a major source of livelihood for the coastal communities which has resulted in a largely unregulated fishery with very high fishing pressure over the last decade (Kaunda-Arara et al. , 2003; Agembe et al. , 2010).

The reproductive activity of fishes also varies among species and from one geographical region to another (Shapiro, 1987; Adams et al ., 2000). For example, spatial variations in spawning seasons has been reported for E. akaara sub-populations in Hong Kong, Taiwan and Fuji (Hong & Zhang, 1994) as well as for E. diacanthus and E. merra in Taiwan, Oman and Okinawa (Lee et al ., 2002; McIlwain et al ., 2006). These variations suggest that reproductive activity cannot be blankly applied across fish stocks in different regions even in the populations of the same species. Consequently, an effective management strategy for

a particular fish species can only be developed from specific bio-ecological data if the efforts to reduce overfishing and over-exploitation are to bear fruit (Myers et al. , 2007).

CHAPTER THREE

3. MATERIALS AND METHODS

Description of the Study Sites

The study was conducted at three selected fish landing sites along south coast with the northern most site, Msambweni straddling 04°30´31.26" S and 039°28´12.97" E, about 70 km south of Mombasa city; and Vanga on the southern border with Tanzania at

04°40´16.11" S and 039°13´36.96" E. Shimoni, the third site was selected as the central station between Msambweni and Vanga, and straddles 04°38´52.67" S and 039°22´50.55" E

(Figure 1).

`Figure 1: A map of Kenya (Inset) showing the location of the study sites; Vanga, Shimoni and Msambweni in South Coast, Kenya

Research design

The present study employed a stratified random sampling design (SRSD). Data was collected from samples landed by the small scale artisanal fisheries as well as from experimental surveys at selected fishing grounds.

Sampling was conducted over a period of eight months with three (3) days of survey every month at each of the three selected sites; Vanga, Shimoni and Msambweni. All fishers targeting groupers were sampled at each site and the catch sorted to species level for each fishing vessels or fisher. Data on species composition, abundance, length-weight measurements and reproductive activity was determined for each species, and sex-ratios,

Fulton condition factor (K F) and gonado-somatic indices (GSI) calculated for each species.

Secondly, experimental surveys were conducted to ascertain the distribution of the landed grouper species in the three fishing grounds. The experimental surveys employed a long- swim underwater visual census (UVC) method adapted from Choat & Pears (2003). The

UVC survey method employs detailed search for species along a 100-m transect with slow timed swims of 45-min. duration at average search speeds of 30 m/min. On either side of the transect line, a 10-m bandwidth was surveyed for the larger-sized Epinephelus individuals while a 2.5-m bandwidth was used for the smaller, cryptic and roving individuals (Figure 2).

Each transect portion was viewed once and all encountered Epinephelus grouper individuals identified to species level and counted. All the UVCs were conducted using the same observer and data recorded onto a prepared water proof data slate to ensure consistency.

NB : Swim observer (= student) searches the central 5 m width Larger sized band for small, cryptic, and Individuals 10 m roving genus individuals while also concurrently surveying a 2.5m band of 10 m to either side for Small Individuals the larger sized individuals (Adapted from Pears, 2009). Swim Observer

Figure 2: Diagram illustrating the long-swim transects method used in the UVC of the Epinephelus groupers in south-coast Kenya

Field Sampling

Field sampling was conducted on a monthly basis during December 2013 through July,

2014. At the fishing village beach, all fish landings from the small-scale artisanal fishers were sorted to species level using keys and guides from Smith & Heemstra (1986);

Heemstra & Randall (1993) and Anam & Mostarda (2012), and all specimens of the

Epinephelus species set aside for further analysis. Data on species composition and abundance were computed from the recorded data from the landings. All Epinephelus individuals were measured for total length (TL, cm) to the nearest 0.1 cm using a measuring board while body weight (BW, g) was measured to the nearest 0.01g on a top loading Salter digital balance model 2010.Further, the specimens were dissected (Plate 2) for sex determination and sexual maturity determined based on macroscopic examination of the gonads using protocols adapted from Rhodes & Sadovy (2002) for Epinephelus polyphekaidon Bleeker, 1849. The ovaries and testes were then further classified for gonadal maturity based on the developmental stages described by both Ferreira (1995) and

Adams (2003).

Plate 2: Photo showing grouper samples being dissected to remove gonads for use in sexing and maturity staging

Processing of the Gonad samples

The gonads from each individual were immediately frozen whole for latter processing on arrival in the laboratory or preserved separately in a bottle using 10% phosphate buffered formalin and (Adams, 2003). On arrival in the laboratory, any frozen gonads were thawed and preserved in 10% phosphate buffered formalin. For analysis, each fixed pair of gonads was dried of excess fixative and the weights measured to the nearest 0.01 g. Where only one gonad lobe was available due to damage during processing, the total gonad weight for the individual was estimated by multiplying the mass of the single lobe by two, assuming that the two lobes are equal in size for groupers as reported by Adams (2003). Additional features used for determination of the sexual maturity stages of the Epinephelus included gonad vascularization and relative thickness of the gonad walls as indicators of prior spawning (Ramadan & El-Halfawy, 2007). The gonads were then classified as shown in

Table 1.

Table 1: Criteria 1 used in the determination of maturity stages of grouper species in the present study

a) Ovaries

Maturity Stage Macroscopic features I = Immature Ovary small, strand-like, compact, pink or cream; oocytes (eggs) not clearly distinct; not obviously different from immature or inactive males.

II = Maturing Ovary relatively small but rounded, less strand-like in appearance, grayish with thickened gonad wall; eggs not clearly distinct and small; Not clearly different from mature males prior to the development of yolk within the eggs.

III = Mature, active Ovary large and grayish with transparent gonad wall; large yolky eggs becoming clearly visible and tightly packed.

IV-V = Mature, ripe Ovary relatively large, clear, watery (hydrated) eggs visible through wall; typical of individuals just prior to spawning; egg release possible with application of light abdominal pressure. VI = Post-spawn (Spent) Ovary flaccid with obvious capillaries (small blood vessels); few eggs still visible.

b) Testes

I = Immature / inactive Testes not obviously different from immature females (see the description of immature females). II = Maturing Early Male II individuals are indistinguishable from Female II. Single blood vessel on ventral side. No sperm extricable when pressed lightly. III = Mature, active Testes expanding and becoming rounded and large; grayish in appearance; early maturing individuals are not clearly different from maturing females until milt (sperm) becomes evident in the sperm sinus along the gonad wall.

IV-V = Mature, ripe Testes large and white with sperm visible in sinuses along the gonad wall; milt release with light abdominal pressure.

VI = Post-spawn (Spent) Testes flaccid and bloody; sperm release still possible on application of abdominal pressure.

1 Adapted from Adams (2003)

Determination of Species composition and abundance

All the fish landings at each of the selected sites were sorted to species level and all individual of the Epinephelus species further sorted and counted for determination of species composition and abundance. The species abundance was computed from data collected on total numbers of each species.

Determination of Length-Weight Relationships (LWRs)

The length-weight relationship for each species was calculated for each species using the data on individual species length (TL, cm) and weight (BW, g) using the equation: W=aL b

(Froese, 2006); where the W is the body weight (BW, g), L the total length (TL, cm), "a" the intercept of the regression curve and "b" is the slope of the curve, or regression coefficient.

The parameters "a" and "b" of the length-weight relationship were estimated by linear regression analysis based on natural logarithms: ln(W)=ln(a) + b ln(L). The coefficient of determination (r2) was used as an indicator of the quality of the linear regressions (Scherrer,

1984). Further, 95% confidence limits of the parameters "b"(CL 95%) were computed using the equation: CL= b ± (1.96 x SE) where SE is the standard error of "b". To determine if the growth pattern was isometric (b=3), negative allometric (b<3) or positive allometric (b>3), a test for significant variation of the computed "b" value from 3 was conducted using

Student’s t-test using the equation by Sokal & Rohlf (1987): ts =(b-3)/SE, where ts is the t- test value, "b" the slope and SE the standard error of the slope "b" (Sokal and Rohlf, 1987;

Somers, 1991; Zar, 2010). In all cases, the statistical analyses were only considered significant at a level where p < 0.05.

Estimation of Fulton condition factors

Fulton condition factor (K F) values were calculated for each species using the equation

-3 described by Cone (1989): KF =1000W.L where W is the body weight (BW, g) and L is

the total length (TL, cm).The scaling factor of 1000 is used to bring the KF close to unit

(Froese, 2006).

Determination of Gonadosomatic indices (GSI, %)

Gonado-somatic index (GSI, %) for each species of the Epinephelus groupers was calculated using the equation adapted from Hossain et al. (2012) where GSI (%) =

100.GW/BW where GW and BW are the gonad and body weights (g) respectively. The

Temporal variations in the GSI (%) values for each species were used to determine the reproductive activity for both males and females and gauge the spawning period (Hossain et al. , 2012). Sex ratios were calculated as the ratio of the number of females to males for each species that recorded more than single catches. The results were then compared with the expected natural sex ratio of 1:1 using Chi -square test (Zar, 2010).

Determination of Reproductive Activity of Epinephelus species

The reproductive activity for each species was determined using the gonado-somatic index

(GSI) results, Fulton ’s condition factor (K F) and sex ratios.

Data and Statistical Tests for Significance

All statistical analyses were conducted using Microsoft ®Excel 2010 and Minitab ® (version

14) software. For all statistical tests, significance was determined at α = 0.05.

CHAPTER FOUR

4. RESULTS

Species composition and abundance

A total of 401 Epinephelus grouper specimens belonging to 30 different species were collected from the three study sites of Msambweni, Shimoni and Vanga in south coast

Kenya. The species comprised of E. acanthistus Gilbert, 1892; E. areolatus Forsskål, 1775;

E. bentoides Valenciennes, 1828; E. chabaudi Castelnau, 1861; E. chlorostigma

Valenciennes, 1828; E. coeruleopunctatus Bloch, 1790; E. coioides Hamilton, 1822; E. diacanthus Valenciennes, 1828; E. epistictus Temminck & Schlegel, 1842; E. fasciatus

Forsskål, 177 5; E. flavocaeruleus Lacepède, 1802; E. Fuscoguttatus Forsskål, 1775; E. hexagonatus Forster, 1801; E. lanceolatus Bloch, 1790; E. longispinis Kner, 1864; E. macrospilos Bleeker, 1855; E. malabaricus Bloch & Schneider, 1801; E. melanostigma

Schultz, 1953; E. merra Bloch, 1793; E. miliaris Valenciennes, 1830; E. Morrhua

Valenciennes, 1833; E. multinotatus Peters, 1876; E. poecilonatus Temminck &Schlegel,

1842; E. polyphekadion Bleeker, 1849; E. rivulatus Valenciennes, 1830; E. socialis Günther,

1873; E. spilotoceps Schultz, 1953; E. tauvina Forssk ål, 1775; E. tukula Morgans, 1959 and

E. Undulosus Quoy & Gaimard, 1824. All the species recorded from the small-scale fisheries landings data were also confirmed from the underwater visual census (UVC) surveys except for two species; E. chabaudi , and E. morrhua which were absent in the

UVCs. Spatially, 77 of the Epinephelus specimens belonging to 20 different species were from Msambweni, 223 belonging to 23 species from Shimoni, and 101 specimens belonging to 18 species from Vanga fish landing site. The number of individuals varied between species and across sites with E. fasciatus being the most abundant in both the landed and visually observed specimen recordings with 54 and 64 individuals, respectively. The E. undulosus recorded the lowest numbers of individuals in both cases (Figure 3).

Landings UVC counts

35 17

18 Number ofindividuals Number

0 E. merra E. E. tukula E. E. miliaris E. E. tauvina E. E. socialis E. E. morrhua E. E. rivulatus E. E. coioides coioides E. E. chabaudi E. E. areolatus E. E. epistictus E. E. fasciatus E. E. undulosus E. E. bentoides bentoides E. E. diacanthus E. E. spilotoceps E. E. acanthistus E. E. longispinis E. E. lanceolatus lanceolatus E. E. malabaricus E. E. chlorostigma E. E. multinotatus E. E. fuscoguttatus E. E. macrospilos macrospilos E. E. poecilonatus poecilonatus E. E. hexagonatus hexagonatus E. E. polyphekadion E. E. melanostigma melanostigma E. E. flavocaeruleus flavocaeruleus E. E. coeruleopunctatus E. Species

The number of individuals for each Epinephelus species also varied considerably within and between the study sites (Table 2). Thus, during the analysis, only fifteen (15) species were found to record >10 specimens in terms of numbers during the entire study period. Among these species, E. fasciatus was the most abundant with 54 specimens recorded over the 8 months period. Ten (10) of the specimens were recorded from Msambweni with 26 and 18 specimens being recorded from Shimoni and Vanga landing sites, respectively. The second most abundant species was E. malabaricus with 36 specimens, E. coeruleopunctatus (31),

E. longispinis (28), E. areolatus (26), E. multinotatus (24), E. chlorostigma (21), E. merra

(17), E. tauvina (16) and E. coioides (15) while E. hexagonatus , E. macrospilos , E. spilotoceps and E. tukula recorded 14 specimens each, and E. miliaris recorded 13 specimens from the three landing sites during the survey period. The rest of the species recorded <10 specimens for each of the species.

During the present survey, it was also noted that two of the landed grouper species; E. chabaudi and E. Morrhua were not reported from the underwater visual census (UVCs).

Similarly, the numerical counts of the species was also lower in the UVCs compared to the statistics from the small-scale landings with only 14 species recording counts >10 per species during the entire period of study with E. fasciatus still being most abundant with 64 specimens. This was followed by E. coeruleopunctatus (43), E. areolatus (26), E. chlorostigma (18), E. malabaricus and E. tauvina (17 specimens each), E. longispinis, E. merra, E. tukula, and E. Fuscoguttatus (12 specimens each), E. coioides, E. hexagonatus, and

E. spilotoceps (11 specimens each) and E. multinotatus (10).

Table 2: Number of landed specimens of Epinephelus groupers by species and site during the present survey in south coast Kenya

No. Species Msambweni Shimoni Vanga Total

1 Epinephelus acanthistus 0 0 4 4

2 Epinephelus areolatus 0 20 6 26

3 Epinephelus bentoides 0 4 0 4

4 Epinephelus chabaudi 1 0 0 1

5 Epinephelus chlorostigma 3 10 8 21

6 Epinephelus coeruleopunctatus 5 18 8 31

7 Epinephelus coioides 0 12 3 15

8 Epinephelus diacanthus 2 4 0 6

9 Epinephelus epistictus 2 0 3 5

10 Epinephelus fasciatus 10 26 18 54

11 Epinephelus flavocaeruleus 8 0 0 8

12 Epinephelus fuscoguttatus 3 3 1 7

13 Epinephelus hexagonatus 4 10 0 14

14 Epinephelus lanceolatus 0 4 2 6

15 Epinephelus longispinis 6 13 9 28

16 Epinephelus macrospilos 0 10 4 14

17 Epinephelus malabaricus 4 20 12 36

18 Epinephelus melanostigma 2 3 2 7

19 Epinephelus merra 1 10 6 17

20 Epinephelus miliaris 0 4 9 13

21 Epinephelus morrhua 1 0 0 1

22 Epinephelus multinotatus 5 17 2 24

23 Epinephelus poecilonatus 0 6 0 6

24 Epinephelus polyphekadion 0 1 0 1

25 Epinephelus rivulatus 0 6 0 6

26 Epinephelus socialis 1 0 0 1

27 Epinephelus spilotoceps 6 8 0 14

28 Epinephelus tauvina 4 10 2 16

29 Epinephelus tukula 8 4 2 14

30 Epinephelus undulosus 1 0 0 1

Total 77 223 101 401

Analysis of the landings and UVCs data for the two monsoon seasons influencing fisheries and fishing activities on the Eastern Coast of Africa i.e. the North East Monsoon Season

(NEM) which runs from December to March, and the South East Monsoon Season (SEM) running from April to July, showed that both species composition and abundance (numerical abundance of individuals) varied considerably suggesting an influence of the seasons on both species diversity and abundance. Notably, seven (7) of the recorded species including E. chabaudi, E. coioides, E. polyphekadion, E. rivulatus, E. undulosus, E. morrhua, and E. miliaris were landed only landed during the southeast monsoon (SEM, April-July) season.

Similarly, total landings were also higher during this season, with a total of 286 individuals recorded during the SEM season compared to 115 recorded in the NEM season (Table 3).

Table 3: Variations in the numerical abundance of landed specimens for each specimen in NEM and SEM seasons during the present study # Species NEM Season (Dec / March) SEM Season (April / July)

1 E. acanthistus 1 3 2 E. areolatus 1 25 3 E. bentoides 1 3 4 E. chabaudi 0 1 5 E. chlorostigma 1 20 6 E. coeruleopunctatus 13 18 7 E. coioides 0 15 8 E. diacanthus 1 5 9 E. epistictus 3 2 10 E. fasciatus 10 44 11 E. flavocaeruleus 1 7 12 E. fuscoguttatus 5 2 13 E. hexagonatus 1 13 14 E. lanceolatus 1 5 15 E. longispinis 12 16 16 E. macrospilos 2 12 17 E. malabaricus 19 17 18 E. melanostigma 1 6 19 E. merra 7 10 20 E. miliaris 0 13 21 E. morrhua 0 1 22 E. multinotatus 12 12 23 E. poecilonatus 1 5 24 E. polyphekadion 0 1 25 E. rivulatus 0 6 26 E. socialis 1 0 27 E. spilotoceps 3 11

28 E. tauvina 13 3 29 E. tukula 5 9 30 E. undulosus 0 1

Total number of individuals 115 286

Length-weight relationships (LWRs) Analyses

During the survey period, the sizes of the landed specimens of the Epinephelus groupers from the Indian Ocean waters of south coast Kenya ranged from 10.0 to 77.9 cm TL with corresponding body weights (BW, g) of from 199.0 to 2804.0 g. In the smaller sized (small bodied) Epinephelus grouper species comprising E. acanthistus, E. areolatus, E. bentoides, E. chlorostigma, E. coeruleopunctatus, E. diacanthus,E. fasciatus,E. hexagonatus, E. longispinis,

E. macrospilos, E. melanostigma , E. merra, E. miliaris, E. poecilonatus , E. rivulatus , E. socialis , E. spilotoceps , E.tauvina , and E. undulosus , the sizes of the specimens ranged from13.0 to 31.0 cm TL with corresponding body weights (BW, g) ranging from 199.0 to

996.0 g. It was noted that majority of the landed specimens of these small bodied species were however above 22.0 cm TL suggesting a healthy fishery for these smaller bodied Epinephelus grouper species. In the large sized (big bodied) species, the sizes ranged from 17.4 to 77.9 cm

TL with corresponding body weights (BW, g) of 298.0 to 2,804.0 g BW. Due to the low numerical counts of some of the species, analysis of LWRs was only conducted on 25 of the

Epinephelus grouper species which recorded > 3 specimens in the landings from the small- scale reef fisheries off the south coast Kenya Indian Ocean waters. The results of the LWRs analysis are shown in Figures 4-6. However, the analysis of the LWR data for E. tukula showed a very poor relationship (r2 < 0.3) and therefore both the analysis and graph were discarded.

a) Epinephelus acanthistus b) Epinephelus areolatus 500 y = 31.89x 0.779 y = 29.32x 0.891 450 R² = 0.998 640 R² = 0.852 400 350 440 Weight (g) Weight Weight (g) Weight 300 240 15 25 35 10 20 30 40 Total Length (cm) Total Length (cm)

c) Epinephelus bentoides d) Epinephelus chlorostigma y = 65.52x 0.554 304 y = 82.20x 0.442 R² = 0.900 294 294 R² = 0.938 284 284

Weight (g) Weight 274 274 (g) Weight 264 264 12 14 16 14 16 18 Total Length (cm) Total Length (cm)

g) Epinephelus diacathus h) Epinephelus fasciatus 0.706 y = 46.16x 0.696 250 y = 38.53x 380 R² = 0.959 R² = 0.704 230 330 210 Weight (g) Weight Weight (g) Weight 190 280 9 11 13 15 13 18 23 Total Length (cm) Total Length (cm)

i) Epinephelus flavocaeruleus j) Epinephelus fuscoguttatus y = 80.99x 0.428 2679 338 R² = 0.959 2.803 2179 y = 0.012x R² = 0.728 318 1679 Weight (g) Weight Weight (g) Weight 1179 298 679 20 25 30 45 65 Total Length (cm) Total Length (cm) Figure 4: Length-weight relationships’ for E. acanthistus, E. areolatus, E. bentoides, E. chlorostigma E. coeruleopunctatus, E. coioides, E. diacanthus, E. fasciatus, E. flavocaeruleus, and E. fuscoguttatus from the small-scale fisheries in south coast, Kenya

k) Epinephelus hexagonatus l) Epinephelus lanceolatus 1.71 y = 27.84x 0.83 y = 2.345x 1152 280 R² = 0.820 R² = 0.836 260 952 240 752

Weight (g) Weight 220 552 Weight (g) Weight 200 352 10 15 20 30 40 Total Length (cm) Total Length (cm)

m) Epinephelus longispinis n) Epinephelus macrospilos 340 y = 105.3x 0.379 R² = 0.886 0.961 340 290 y = 24.00x R² = 0.842 240 290 Weight (g) Weight Weight (g) Weight 190 240 10 15 20 11 21 Total Length (cm) Total Length (cm)

o) Epinephelus malabaricus p) Epinephelus melanostigma

925 390 y = 132.8x 0.302 370 R² = 0.952 725 y = 9.284x 1.182 350 R² = 0.891 330

Weight (g) Weight 525 Weight (g) Weight 310 325 290 20 40 60 15 20 25 Total Length (cm) Total Length (cm) q) Epinephelus merra 600 r) Epinephelus miliaris 599 1.010 500 y = 17.42x y = 0.091x 2.783 R² = 0.943 499 R² = 0.734 400 399 Weight (g) Weight 300 Weight (g) Weight 299 200 18 20 22 24 13 23 33 Total Length (cm) Total Length (cm)

Figure 5: Length-weight relationships’ for E. hexagonatus, E. lanceolatus E. longispinis, E. macrospilos, E. malabaricus, E. melanostigma, E. merra, and E. miliaris from the small-scale fisheries in south coast, Kenya

s) Epinephelus multinotatus t) Epinephelus poecilonatus

1.237 380 680 y = 10.87x y = 69.39x 0.579 R² = 0.829 360 R² = 0.879 580 340 Weight (g) Weight Weight (g) Weight 480 320 380 300 17 22 27 13 23 Total Length (cm) Total Length (cm)

u) Epinephelus rivulatus v) Epinephelus spilotoceps 325 y = 13.91x 1.2 250 y = 33.81x 0.761 R² = 0.768 R² = 0.965 315 230 305 Weight (g) Weight Weight (g) Weight 210 295 190 285 10 12 14 12 13 14 Total Length (cm) Total Length (cm)

w) Epinephelus tauvina y = 107.6x 0.335 335 R² = 0.494 315 295 275 Weight (g) Weight 255 235 12 17 22 Total Length (cm)

Figure 6: Length-weight relationships’ for E. multinotatus, E. poecilonatus E. rivulatus, E. spilotoceps, and E. tauvina from the small-scale fisheries in south coast, Kenya

Using the Students t-test, LWR analyses revealed negative allometric growth (b < 3) for all species of the Epinephelus groupers except for two species; E. Fuscoguttatus and E. miliaris which recorded LWR estimates close to isometric growth (b close to 3; b = 2.804 (Figure 4-

“j”) and 2.783 (Figure 5-“r”), respectively. The regression coefficient of determination (r2) values for 23 species were significantly positive (r2 > 0.6) while E. tauvina and E. tukula , showed lower values for r2; 0.49 and 0.23, respectively. Regression analysis of the L-W relationships for 25 species revealed significant differences in the initial body weights

(intercept “a”) (t= 4.480; p < 0.01) but no significant differences in the growth pattern or slopes (isometric growth test “b”) (t= 1992.2; p = 0.59).

Reproductive Activity of Epinephelus groupers

The reproductive activity of the Epinephelus grouper species was deduced from the sex-ratios,

Fulton condition factor values and gonado-somatic indices. The sex ratios, mean Fulton ’s condition factors (K F) and pooled monthly gonado-somatic indices for the 30 species analyzed species in the present study are shown in Table 4, Table 5 and Figure 8, respectively. All had varying sex ratios with twelve (12) species including E. acanthistius , E. areolatus , E. chlorostigma , E. coeruleopunctatus , E. fasciatus , E. hexagonatus , E. macrospilos , E. malabaricus , E. miliaris , E. multinotatus , E. tauvina and E. tukula having ratios that were different from the expected M: F ratio of 1:1 (Table 4).

Table 4: Sex ratios of Epinephelus grouper species from the small-scale fisheries of south coast Kenya; p-value = significance level (α = 0.05); χ2- calculated chi -square statistic; *significantly different from the expected 1:1 ratio

No. Species N Sex ratio (M: F) χ2 df p-value

1 Epinephelus acanthistus 4 0.0: 4.0 4.000 1 ---

2 Epinephelus areolatus 26 1.0: 3.3 7.538 1 0.01*

3 Epinephelus bentoides 4 1.0: 3.0 1.000 1 ---

4 Epinephelus chabaudi 1 0.0: 1.0 1.000 1 ---

5 Epinephelus chlorostigma 21 1.0: 3.2 5.762 1 0.02*

6 Epinephelus coeruleopunctatus 21 1.0: 3.4 9.323 1 0.01*

7 Epinephelus coioides 15 1.0: 2.8 3.267 1 0.07

8 Epinephelus diacanthus 6 1.0: 5.0 2.667 1 ---

9 Epinephelus epistictus 5 1.0: 1.5 0.200 1 0.66

10 Epinephelus fasciatus 54 1.0: 2.9 12.532 1 0.01*

11 Epinephelus flavocaeruleus 8 1.0: 3.0 2.000 1 0.16

12 Epinephelus fuscoguttatus 7 1.0: 2.5 1.286 1 0.26

13 Epinephelus hexagonatus 14 1.0: 3.7 4.571 1 0.03*

14 Epinephelus lanceolatus 6 1.0: 5.0 2.667 1 ---

15 Epinephelus longispinis 28 1.0: 1.8 2.286 1 0.13

16 Epinephelus macrospilos 14 1.0: 3.7 4.571 1 0.03*

17 Epinephelus malabaricus 36 1.0: 4.1 13.412 1 0.01*

18 Epinephelus melanostigma 7 1.0: 6.0 3.571 1 0.06

19 Epinephelus merra 17 1.0: 1.8 1.471 1 0.23

20 Epinephelus miliaris 13 1.0: 3.3 3.769 1 0.05*

21 Epinephelus morrhua 1 0.0: 1.0 1.000 1 0.32

22 Epinephelus multinotatus 24 1.0: 5.0 10.668 1 0.01*

23 Epinephelus poecilonatus 6 1.0: 5.0 2.667 1 0.10

24 Epinephelus polyphekadion 1 0.0: 1.0 1.000 1 0.32

25 Epinephelus rivulatus 6 1.0: 2.0 0.667 1 0.41

26 Epinephelus socialis 1 0.0: 1.0 1.000 1 ---

27 Epinephelus spilotoceps 14 1.0: 2.5 2.571 1 0.11

28 Epinephelus tauvina 16 1.0: 3.0 4.000 1 0.05*

29 Epinephelus tukula 14 1.0: 3.7 4.571 1 0.03*

30 Epinephelus undulosus 1 0.0: 1.0 1.000 1 ---

Twelve of the species had sex ratios which were not significantly different from the expected

M: F ratio of 1:1. The highest sex ratio amongst this group was observed in E. melanostigma where six females had only one male. This was followed by E. diacanthus , E. lanceolatus and

E. poecilonatus rations where one male had five females. The species with the least sex ratio was observed in E. rivulatus where one male had two females. Seven species including E. acanthistus , E. bentoides , E. chabaudi , E. morrhua , E. polyphekadion , E. socialis , and E. undulosus p-values were not calculated as their total specimen numbers were not reaching five

(5) and thus not fitting the Chi -square criteria.

The overall maturity stages of the Epinephelus grouper species varied throughout the entire

study period. Thus, majority of the species collected during December through March that

included Epinephelus acanthistius, E. chabaudi, E. epistictus, E. fuscoguttatus, E. lanceolatus,

E. morrhua, E. polyphekadion and E. undulosus reported only immature (stage I-II)

specimens. During this period covering from December 2013 to March 2014, all samples

collected from 248 individuals based on the gonado-somatic indices shown for the females

(Figure 8a) and males (Figure 8b) accounting for 61.9% of the total samples collected were all

immature (Stage I and II). However, towards the end of April, there was a gradual increase in

the percentage of mature individuals for most of the species with peak percentages recorded during June and July. Maturity stage-II was recorded throughout the study period. The

"mature" stages (Stage-III, VI and V) as well as "spent" maturity stage-VI were only recorded towards the end of April and through the months of May to July with the latter months recording higher percentages of the Stage III and IV individuals especially for E. areolatus, E. chlorostigma, E. coeruleopunctatus, E. coioides, E. diacanthus, E. fasciatus, E, flavocaeruleus, E. hexagonatus, E, longispinis, E. macrospilos, E. malabaricus, E. melanostigma, E. merra, E. miliaris, E. multinotatus, E. poecilonatus, E. rivulatus, E. socialis,

E. spilotoceps, E. tauvina, and E. tukula which accounted for 44.6% and 59.8 % of the Stage

III-IV males and females, respectively.

The percentage of mature individuals of stage-III was also highest during May-July period, accounting for 19.7% (79 specimens) of the recorded 401 individuals. Specimens of E. areolatus, E. bentoides, E. fasciatus, E, flavocaeruleus, E. hexagonatus, E, longispinis, E. macrospilos, E. poecilonatus and E. spilotoceps in the stage IV-V maturity stages accounted for 16.7 % (67 specimens) of the total recorded samples whereas stage (VI) individuals of E. fasciatus, E. spilotoceps, E. chlorostigma and E. macrospilos accounted for 1.7% (7 specimens) of the total recorded number of samples.

100.0

(a)

80.0 I II

60.0 III IV V

Frequency (%) Frequency 40.0 VI

20.0

0.0 Dec Jan Feb Mar Apr May Jun Jul

100

(b) 80 I II 60 III IV V Frequency (%) Frequency 40

0 Dec Jan Feb Mar Apr May Jun Jul

Figure 7: Monthly maturity stages between female and male Epinephelus grouper species sampled during the study.

Mean Fulton condition factor (K F) values calculated during the study varied among the species (Table 5). Two species, E. coeruleopunctatus and E. fasciatus, had mean monthly KF values ranging between 10.4 and 32.5 with their lowest values observed in December. The conditions progressively increased and in July E. coeruleopunctatus and E. fasciatus had peaks of KF (Mean ± SE) = 18.4 ± 0.5 and 32.5 ± 1.7, respectively. Epinephelus undulosus had the lowest mean KF of 3.0 ± 0.0 (Mean ± SE) amongst the small bodied grouper species.

Among the larger bodied species, E. multinotatus had the highest mean condition factor (KF) of 31.3 ± 0.3 to 39.4 ± 0.3 (Mean ± SE), followed by E. morrhua (28.0 ± 0.0) and E. epistictus

(15.6 ± 4.8 to 18.3 ± 0.0). The lowest mean KF among this larger bodied Epinephelus groupers was observed in case of E. tukula in January, followed by E. poyphekadion in June with Mean

± SE values of 2.3 ± 2.0 and 3.0 ± 0.0 respectively (Table 5).

Table 5: Monthly Fulton Condition Factor (KF) for species of the Epinephelus groupers landed by the small-scale marine fisheries in South-coast Kenya

Mean Monthly Fulton Condition Factor (KF) (Mean ± SE) No. Species Dec-2013 Jan-014 Feb-014 Mar-2014 Apr-2014 May-2014 June-2014 July- 2014

1 Epinephelus acanthistus 14.1 ± 0.0 - - - 16.3 ± 0.0 - 17.5 ± 0.0 20.5 ± 0.0 2 Epinephelus areolatus - - 13.0 ± 0.0 - 12.9 ± 2.5 13.3 ± 2.8 13.6 ± 3.3 15.4 ± 0.3 3 Epinephelus bentoides - - - 30.0 ± 0.0 - - 32.2 ± 0.0 33.0 ± 1.4 4 Epinephelus chabaudi - - - - - 9.0 ± 0.0 - -

5 Epinephelus chlorostigma - 10.0 ± 0.0 - - 11.3 ± 0.4 12.8 ± 0.2 14.8 ± 1.0 16.0 ± 0.3

6 Epinephelus coeruleopunctatus 10.4 ± 0.0 11.6 ± 0.5 13.6 ± 4.1 15.0 ± 0.5 16 ± 0.0 16.3 ± 0.3 17.0 ± 0.0 18.4 ± 0.5 32

7 Epinephelus coioides - - - - - 13.6 ± 4.1 14.8 ± 1.0 16.0 ± 0.3 8 Epinephelus diacanthus - - - 12 ± 0.0 - 13.2 ± 0.0 14.0 ± 0.6 - 9 Epinephelus epistictus - - 15.6 ± 4.8 - - 18.3 ±0.0 18.3 ±0.0 - 10 Epinephelus fasciatus 14.8 ± 1.0 - 16.0 ± 0.3 17.0 ± 0.0 17.5 ± 0.5 21.3 ± 0.1 26.2 ± 1.1 32.5 ± 1.7 11 Epinephelus flavocaeruleus - - 13.0 ± 0.0 - - - 15.4 ± 0.3 - 12 Epinephelus fuscoguttatus - - - 4.1 ± 0.3 - 5.0 ± 0.0 - 5.0 ± 0.0 13 Epinephelus hexagonatus 15 ± 0.0 - - - 27.0 ± 11 - 34.8 ± 0.8 - 14 Epinephelus lanceolatus - 14 ± 0.0 - - - - - 16.0 ± 0.2 15 Epinephelus longispinis 12.5 ± 5.1 - - 15.2 ± 13.2 - - 25.3 ± 0.5 29.5 ± 0.5 16 Epinephelus macrospilos 16.0 ± 0.0 - - 18.0 ± 0.0 - - 23.3 ± 0.3 25.9 ± 0.3

Mean Monthly Fulton Condition Factor (KF) (Mean ± SE ) No. Species Dec-2013 Jan-2014 Feb-2014 Mar-2014 Apr-2014 May-2014 June-2014 July-2014 17 Epinephelus malabaricus - - 5.5 ± 1.3 8.5 ± 0.3 - - 8.7 ± 2.0 11.2 ± 0.8 18 Epinephelus melanostigma - - 17.0 ± 0.0 - - 19.8 ± 0.3 - - 19 Epinephelus merra - 10.2 ± 8.8 - - - - 18.0 ± 0.6 - 20 Epinephelus miliaris - - - - - 18.3 ± 5.0 - 23.8 ± 0.3 21 Epinephelus morrhua - - - - 28.0 ± 0.0 - - - 22 Epinephelus multinotatus 31.3 ± 0.3 - 34.0 ± 0.4 - - 36.3 ± 0.4 - 39.4 ± 0.3 33

23 Epinephelus poecilonatus - - - 18.0 ± 0.0 - - - 19.5 ± 0.5 24 Epinephelus polyphekadion ------3.0 ± 0.0 - 25 Epinephelus rivulatus ------46.4 ± 0.5 26 Epinephelus socialis - - - 42.0 ± 0.0 - - - - 27 Epinephelus spilotoceps - 14.1 ± 0.0 15.7 ± 0.0 16.2 ± 0.0 - 17.0 ± 6.6 - 24.0 ± 0.3 28 Epinephelus tauvina - - 17.3 ± 4.6 23.0 ± 0.3 - 24.0 ± 0.0 25.2 ± 0.0 26.9 ± 0.0 29 Epinephelus tukula - 2.3 ± 2.0 - - - - - 10.8 ± 0.4 30 Epinephelus undulosus - - - - - 3.0 ± 0.0 - -

CHAPTER FIVE

5. DISCUSSION

Species composition and abundance of Epinephelus groupers

A total 30 species of the Epinephelus groupers were recorded in the marine waters of the south coast marine waters of Kenya with eleven (11) of the species being recorded in all the three sites studies. This may partly be attributed to similarity in the nature of the marine habitats in the three sites as reported by Agembe (2009). The Msambweni-Shimoni-Vanga continental shelf comprises a fringing reef spanning which would provide similar macro- habitats suitable for the species of the Epinephelus groupers.

Minor differences in one micro-habitat to the next due to topographic complexity (Bostford et al ., 2007) may have, similarly have excluded the other nineteen (19) species from particular sites / habitats. For example, E. flavocaeruleus, E. chabaudi, E. socialis, E. undulosus, and E. morrhua were only recorded from Msambweni but were absent in the southern sites of Shimoni and Vanga. Similarly, E. polyphekadion, E. rivulatus, E. bentoides, and E. Poecilonatus were reported from the Shimoni site but were absent in both sites north and south of Shimoni; in Msambweni and Vanga, respectively. Interestingly, E. acanthistus was only reported from Vanga and was notably absent in the northern landings sites of Shimoni and Msambweni. Some species were only recorded in two of the sites; e.g.

E. epistictus was recorded in both Msambweni and Vanga and absent in the central sites of

Shimoni; E. diacanthus, E. spilotoceps and E. hexagonatus in Msambweni and Shimoni and absent in Vanga; E. miliaris, E. areolatus, E. macrospilos, E. coioides and E. lanceolatus recorded in Shimoni and Vanga and missing in the northern site of Msambweni. These patchy distribution patterns of many of the species could be partly attributed to variations in recruitment, anthropogenic influences on habitat quality due to land-based discharges, shipping and maritime activities and fishing amongst other factors (Sale, 2004; Kaunda-

Arara & Rose, 2004). This may therefore explain the exclusion of some species from sites

despite the continuity of the continental and reef structure of the Msambweni-Shimoni-

Vanga ecosystem.

A higher number of species was reported in the Shimoni fishing sites compared to the northern Msambweni and the southern Vanga sites. These variations and the presence of a higher number of species in the Shimoni site may partly be attributed to the closeness of the

Kisite-Mpunguti Marine Protected Areas (MPA) which would contribute to larval reseeding enhancement within this area (Bostford et al ., 2007). The lower number of species in the

Msambweni site compared to the southern Shimoni and Vanga site may partly be attributed to earlier extensive destruction of the reefs in the late 1980s by the Pemba migrant fishers according to Samoilys (1988).

Seasonally, the southeast monsoon (SEM) season reported higher abundances in the majority of the Epinephelus grouper species compared to those recorded during NEM season. This seasonal variation may be explained by the vulnerability of the species to fishing due to their spawning aggregations and settlement (Kaunda-Arara et al. , 2003; Kaunda-Arara & Rose,

2004; Bostford et al. , 2007). Furthermore, the intensity of fishing effort is often lower during

SEM season as a result of the rough nature of the sea and weather conditions which may also be influencing the availability of food at the spawning or refugia sites based on the species- specific life history strategies (Stewart & Jones, 2001; Church et al. , 2005; Robinson et al. ,

2008). Additionally, habitat type, food availability or physical condition tolerances which are influenced by the rough sea conditions and weather may have also influenced the temporal distribution of these Epinephelus species (McClanahan, 1988; Gibson et al. , 1998; Dahlgren

& Eggleston, 2000).

However, due to lack of data on site- or habitat–specific distributions and abundance of these

Epinephelus groupers along the Kenyan coast, it is difficult to specifically point to the particular factors driving these temporal variations in the distribution of these important species. Furthermore, studies on migration patterns of coral reef fishes has not been

extensively studied as compared to other groups of fishes like those including salmonids and anguillids (Patterson et al. , 2001). This has left numerous gaps as to the specific factors that drive spatio-temporal distributions of these Epinephelus species in the marine waters of south coast Kenya. Sale (2002) suggested that movements and initial migrations in reef fishes were mostly restricted to the pelagic larval-stage dispersal phases. Thus, due to the low number of individuals of each species recorded in the present study, use of available biological data for each species appears to be the most reliable approach of formulating management measures that would be capable of enhancing the recovery and conservation of these Epinephelus groupers for their sustainability.

Length-weight relationships

In the present study, analysis of length-weight relationships (LWRs) showed allometric growth pattern for nine out of the 25 recorded Epinephelus grouper species specimens (E. acanthistus, E. bentoides, E. chlorostigma, E. coeruleopunctatus, E. diacanthus, E. flavocaeruleus, E. melanostigma, E. merra and E. rivulatus ). The LWRs regression coefficients were also considerably strong for these nine (9) species (r 2 > 0.90).This apparently high regression coefficients, point to the species isometric growth pattern relationship even where their ‘b’ values are not exactly three (3). This kind of isometric growth relationship may be minor for some species during their early life history aspects, but becomes important in the calculation of metabolic processes (Laurence, 1978; Cone, 1989).

The reasons for these differences are also suspected to be a reflection of the species settlement histories where recruits are not better placed to survive predation (Stewart &

Jones, 2001). Thus, for such protogynous fish species, this indicates that fishing mortality may have caused insufficient males ’ to remain in the reproductive populations as larger individuals are removed from the population for food (Grandcourt et al. , 2006; McClanahan et al. , 2008).

Therefore, although the ‘b’ values for all sampled specimens were not equal to the expected value of ‘3’ as expected for ideal fish; the tests suggest an isometric growth pattern relationship and the variances witnessed in their regression slope values may be attributed to the development of their gonads. The results of this study are therefore in agreement with previous observations reported by Sarkar et al. (2013) that Length-weight relationship of a fish can be affected by several factors including habitat conditions, seasonal effect, stomach fullness, gonad maturity, sex, health, and length size range differences. This had also been earlier supported by statements by both Cone (1989) and Anderson & Gutreuter (1983) that

‘b’ slope values are always stable and does not significantly vary like ‘a’ intercept values which may even vary daily due to the above factors. Thus, from the results of this study, it may be concluded that the Kenyan south coast Epinephelus groupers LWR follow the isometric growth relationship pattern and the observed variations may have resulted from differences in the number of samples used amongst other earlier reported reasons. The study thus provides significant baseline study on the species LWRs that would be useful for further studies to provide species specific biological data for formulating protection and conservation measures within the Kenyan Indian Ocean coastal waters.

Reproductive Activity of Epinephelus groupers

The results in this study seem to suggest that Epinephelus groupers reproductive activity is influenced by sex ratios, condition factors and maturity stages. Sex ratios indicate the species proportion of male and females in the population and are expected to be 1:1 in nature. Any deviation from this ratio may therefore indicate the dominance of one sex over the other as a result of their sexes differential behaviour, environmental conditions, and fishing effects among other reasons (Hawkins & Roberts, 2003; Mackie, 2003; Alonzo &Mangel, 2004; Liu

& Sadovy, 2004). All species in this study had skewed sex-ratios in favour of females and was in agreement with earlier works carried out on groupers by Shapiro (1987); Sadovy

(1996); Rhodes & Sadovy (2002) and Rhodes & Tupper (2007). In fact, Sadovy (1996) and

Rhodes & Tupper (2007) noted that this kind of biased sex-ratios in groupers is a typical characteristic of their hermaphroditic protogynous lifestyle.

The Epinephelus grouper species KF results in this study showed that the small-bodied groupers comprising E. acanthistus, E. areolatus, E. bentoides, E. chlorostigma, E. coeruleopunctatus, E. diacanthus, E. fasciatus, E. hexagonatus, E. longispinis, E. macrospilos, E. melanostigma, E. merra, E. miliaris, E. poecilonatus, E. rivulatus, E. socialis, E. spilotoceps, E. tauvina, and E. undulosus had values ranging from 3.0 to 46.4.

The larger sized body groupers comprising E. chabaudi, E. coioides, E. epistictus, E. flavocaeruleus, E. fuscoguttatus, E. lanceolatus, E. malabaricus, E. morrhua, E. multinotatus, E. polyphekadion, and E. tukula had KF values ranging from 2.3 to 39.4. This showed that the species were not in good conditions as their (K F) values were all less than

1000 (Sarkar et al. , 2013). This poor condition may have resulted from environmental effects; fish sex, age and maturity. This is because condition factor values reflect both physical and biological factors acting upon the fish (Le Cren, 1951; Sarkar et al. , 2013).

However, from the reproductive point of view, the highest condition factor values may also be achieved in some species during spawning (Angelescu et al. , 1958) as was revealed by the study results. However, caution must be exercised not to use condition factor values singularly in determining spawning period as higher condition factor values could equally result from non-spawning activities (Le Cren, 1951). Thus, combination of both indices

(condition and gonado-somatic indices) have been suggested and used by a number of researchers as an appropriate indicator of spawning periods in teleosts to determine the breeding periods of tropical fishes (DeMartini & Lau, 1999; Ekanem, 2000; Allison et al. ,

2008). Therefore, based on the above reports, and taking into consideration that most species during the study had both their peak (K F) and GSI (%) values coinciding in July, it may be logical to state that most Epinephelus species within the Kenyan south coast Indian Ocean waters have their breeding period as from April to July during the SEM season.

The results agree with findings made by Shapiro (1987) that some grouper species generally spawn over 6-8 months with many spawning for between 1-5 months. However, this spawning in SEM is not in agreement to the earlier findings of Nzioka (1979) and Kaunda-

Arara & Ntiba (1997) indicating that Kenyan reef fishes spawn during NEM season. This disagreement may however be attributed to the lunar based spawning activity of the groupers that make it difficult to detect spawning on a larger scale as is applicable to other fish species

(Shapiro, 1987). The findings thus provide firsthand information on the Kenyan Epinephelus groupers reproductive activity biology for use by both fishery and conservation biologists for future formulation and implementation of protection and conservation measures.

CHAPTER SIX

6. CONCLUSIONS AND RECOMMENDATIONS

Conclusions

The study established presence of 30 Epinephelus grouper species in the Kenyan south coast inshore marine waters. The number of individuals for each species were however low for most species and ranged from between 1 - 64 individuals. The cause for this low numbers was not immediately clear, but increase in fishing due to increased demand for food is suspected to have played a role. The species length-weights showed varied allometric growth relationships with total lengths (TLs) ranging from 10.0 to 77.9 cm and total weights (Ws) that ranged from 199.0 to 2,804.0 g. The observed regression variances (N = 25; t= 4.480; p

< 0.01) for the species (‘a’) intercepts may have therefore resulted from habitat characteristics, food availability, species conditions amongst other reasons as all regression

(‘b’) slopes were not significantly different (N = 25; t = 1992.2; p = 0.59). These Epinephelus grouper species sex ratios, condition factors and GSI appears to greatly influence their reproductive activities as most spawned when having more females, higher (KF) and

(GSI %) values.

Recommendations

From the results of the present study, it is recommended that:-

1) Fisheries resource managers need to integrate the results of current studies on species

specific biological information to develop management plans for sustainable

management of Epinephelus grouper fisheries.

2) More studies should be done to determine the factors driving the spatio-temporal

variations in the abundance of these respective Epinephelus grouper species so as to

provide data and information for formulation of species specific intervention

measures

7. REFERENCES

Adams, S. (2003). Morphological ontogeny of the gonad of three plectropomid species through sex differentiation and transition. Journal of Fish Biology 63: 22-36.

Adams, S., Mapstone, B.D., Russ, G.R. & Davies, C.R. (2000). Geographic variation in the sex ratio, sex specific size, and age structure of Plectropomus leopardus (Serranidae) between reefs open and closed to fishing on the Great Barrier Reef. Canadian Journal of Fisheries and Aquatic Sciences 57: 1448–1458.

Agembe, S.W. (2009). Some aspects of the biology and fishery of groupers (teleostei: Serranidae) in the inshore waters of south coast, Kenya. M.Sc. Thesis. Moi University.

Agembe, S., Mlewa, C.M. & Kaunda-Arara, B. (2010). Catch Composition, Abundance and Length-Weight Relationships of Groupers (Pisces: Serranidae) from Inshore Waters of Kenya. Western Indian Ocean Journal of Marine Science 9(1): 91-102.

Aguilar-Pereira A. (2006). Disappearance of a Nassau grouper spawning aggregation off the Southern Mexican Caribbean coast. Marine Ecology Progress Series 327: 289-296.

Allison, M.E., Sikoki, F.D. and Vincent-Abu, I.F. (2008). Fecundity, Sex ratio, maturity stages, size at first maturity, breeding and spawning of Parailia pellucid (Boulenger, 1901) in the lower Nun River, Niger Delta, Nigeria. Caderno de pesquisa Série Biologia 20 (2):31-40.

Alonzo, S. H. & Mangel, M. (2004). The effects of size-selective fisheries on the stock dynamics of and sperm limitation in sex-changing fish. Fishery Bulletin 102: 1–13.

Anam, R. & Mostarda, E. (2012). Field Identification Guide to the Living Marine Resources of Kenya . FAO Species Identification Guide for Fishery Purposes. Rome, FAO, pp. 170-177.

Anderson, R.O. & Gutreuter, S.J. (1983). On length-weight relationships, Length-weight and associated structural indices. In : Nielsen, L.A., Johnson, D.L. (Eds.), Fisheries Techniques. American Fisheries Society, Bethesda, Maryland, pp. 283–300.

Angelescu, V., Gneri F.S. & Nani, A. (1958). Argentine sea hake (biology and taxonomy) . Secretary Marine Service Hydrogenation Navigational Public, 224pp.

Avise J.C. & Mank, J.E. (2008). Evolutionary Perspectives on Hermaphroditism in Fishes. Sexual Development 3: 152-163.

Bellwood, D.R., Hughes, T.P., Folke, C. & Nystrom, M. (2004). Confronting the coral reef crisis. Nature 429: 827-833.

Bini, L.M., Diniz-Filho, J.A.F., Carvalho, P., Pinto, M.P. & Rangel, T.F.L. (2005). Lomborg and the Litany of Biodiversity Crisis: What the Peer-Reviewed Literature Says. Conservation Biology 19(4):1301-1305.

Bolarinwa, J.B. & Popoola, Q. (2013). Length-Weight Relationships of Some Economic Fishes of Ibeshe Waterside, Lagos Lagoon, Nigeria. Journal of Aquaculture Research Development 5(1):203.

Bostford, L.W., Micheli, F. & Parma, A.M. (2007). Biological and Ecological Considerations in the Design, Implementation and success of MPAs. In: Report and documentation of the Expert workshop on Marine Protected Areas and Fisheries Management: a Review of Issues and Considerations. Rome, 12-14 June 2006. FAO Fisheries Report No.825. Rome, FAO. 332pp.

Bullock, L.H., & Smith, G.R. (1991). Sea basses (Pisces: Serranidae). Memorial Hourglass Cruises 8(2): 1-243.

Campbell, S.J. & Perdede, S.T. (2006). Reef Fish Structure and Cascading Effects in Response to Artisanal Effects in Response to Artisanal Fishing Pressure. Fisheries Research 79: 75-83.

Chan, T., Sadovy, Y. & To, A. (2007). IUCN Red List of Threatened Species Epinephelus bruneus .http://www.iucnredlist.org/search/details.php/64 6/sum (Accessed 10th May 2014).

Choat, J.H. & Pears, R.J. (2003). A rapid quantitative survey method for large vulnerable reef fishes. In: Dione, S. (ed). Monitoring Coral Reef Marine Protected Areas: A practical guide on how monitoring can support effective management of MPAs. Version 1. Australian Institute of Marine Science, Townsville.

Church, J., Samoilys, M., Alidina, H., Waweru, G., Agembe, S. & Kimani, P. [2005]. Coral reef fish spawning aggregations in Southern Kenya. In Western Indian Ocean Proceedings, Mauritius. 40 p.

Coleman, F.C., Koenig, C.C. & Collin, L.A. (1996). Reproductive styles of shallow water groupers (Pisces: Serranidae) in the Eastern Gulf of Mexico and the consequences of fishing spawning aggregations. Environmental Biology of Fishes 47: 129–141.

Colin, P.L. (2012). Timing and Location of Aggregation and Spawning in Reef Fishes . In : Reef Fish Spawning Aggregations: Biology, Research and Management, De Mitcheson, Y. S. and P. L. Colin (Eds.). Springer, New York, USA, pp.: 117-158.

Cone, R.S. (1989). The need to reconsider the use of condition indices in fishery science. Trans-Atlantic American Fishery Society 118 (5): 510-514.

Dahlgren, C.P. & Eggleston, D.B. (2000). Ecological processes underlying ontogenetic habitat shifts in a coral reef fish. Ecology 81: 2227-2240.

DeMartini, E.E. & Lau, B.B. (1999). Morphometric criteria for estimating sexual maturity in two snappers. Etelis carbunculus and Pristipomoides Sieboldii. Journal of Fish Biology 97:449-458.

Dulvy, N.K., Polunin, N.V.C., Mill, A.C. & Graham, N.A.J. (2004). Size structural change in lightly exploited coral reef fish communities: evidence for weak indirect effects. Canadian Journal of Fisheries and Aquatic Sciences 61: 466-475.

Ekanem, S.B. (2000). Some reproductive aspects of Chrysichthys nigrodigitatus (lacepede) from cross River, Nigeria. Naga, ICLARM 2: 2.

Esseen, M. & Richmond, M.D. (2011). Superclass Pisces-Fish.in A Field Guide to the Seashores of Eastern Africa and the western Indian Ocean Islands (ed. Richmond, M.D.) 3rd Edition, pp. 340-379. Sida / WIOMSA.

Ferreira, B.P. (1995). Reproduction of the common coral trout Plectropomus leopardus (Serranidae: Epinephelinea) from the central and southern Great Barrier Reef, Australia. Bulletin of Marine Sciences 56: 653-669.

Froese, R. (2006). Cube law, condition factor and weight–length relationships: history, meta- analysis and recommendations. Journal of Applied Ichthyology 22: 241–253.

Gibson, R.N., Pihl, L., Burrows, M.T., Modin, J., Wennhage, H. & Nickell, L.A. (1998). Diel movements of juvenile plaice Pleuronectes platessa in relation to predators, competitors, food availability and abiotic factors on a microtidal nursery ground. Marine Ecology Progress Series 165: 145-159.

Gillett, R. & Moy, W. (2006). Spear fishing in the Pacific Islands current status and management issues. FAO / Fish Code Review No. 19, Rome, FAO. 72pp.

Grandcourt, E.D., Thabit, Z. and Al Shamsi, F.F. (2006). Biology and assessment of the painted sweetlips (Diagramma pictum (Thunberg, 1792)) and the spangled emperor (Lethrinus nebulosus (Forsskål, 1775)). Southern Arabian Gulf Fishery Bulletin , 104: 75–88.

Gupta, B.K., Sarkar, U.K., Bhardwaj, S.K. & Pal, A. (2011). Condition factor, length-weight and length-length relationships of an endangered fish Ompok pabda (Hamilton 1822) (Siluriformes: Siluridae) from the River Gomti, a tributary of the River Ganga, India. Journal of Applied Ichthyology 27(3): 962-964.

Hawkins, J.P. & Roberts, C.M. (2003). Effects of fishing on sex-changing Caribbean parrot fishes. Conservation Biology 115: 213–226.

Heemstra P.C. & Randall J.E. (1993). Groupers of the World (Family Serranidae, Subfamily Epinephelinae). An Annotated and Illustrated Catalogue of the Groupers, Rock cod, Hind, Coral Grouper and Lyre tail Species Known to Date . FAO Fisheries Synopsis, No. 125: Vol.16. FAO, Rome. 382pp.

Helfman, G.S., Collettee, B.B. & Facey, D.E. (1997). The Diversity of Fishes . Blackwell Science, Massachusetts.

Hong, W.S. and Zhang, Q.Y. (1994). Present status of Epinephelus akaara propagation, seeding fish and larvae culturing study. Marine Science 5: 17–19.

Hossain, M.Y., Jasmine, S., Ibrahim, A.H.M., Ahmed, Z.F., Rahman, M.M. & Ohtomi, J. (2009). Length-weight and length-length relationships of 10 small fish species from the Ganges. Bangladesh Journal of Applied Ichthyology 25: 117-119.

Hossain, M.Y., Jewel, M.A.S., Nahar, L., Rahman, M.M., Naif, A. & Ohtomi, J. (2012). Gonado-somatic index-based size at first sexual maturity of the catfish Eutropiichthys vacha (Hamilton, 1822) in the Ganges River (NW Bangladesh). Journal of Applied Ichthyology 28: 601-605.

Hossain, M.Y., Rahman, M.M., Fulanda, B., Jewel, M.A.S., Ahamed, F. & Ohtomi J. (2011). Length–weight and length–length relationships of five threatened fish species from

the Jamuna (Brahmaputra River tributary) River, northern Bangladesh. Journal of Applied Ichthyology 28(2): 275–277.

Johannes, R.E., Squire, L., Graham, T., Sadovy, Y. & Renguul, H. (1999). Spawning aggregations of groupers (Serranidae) in Palau .Marine Conservation Research Series Publication No. 1. The Nature Conservancy, 144 pp.

Kaunda-Arara, B. & Ntiba, M.J. (1997). The reproductive biology of Lutjanus fulviflamma (Forsskål, 1775) (Pisces: Lutjanidae) in Kenyan inshore marine waters. Hydrobiologia 353: 153-160.

Kaunda-Arara, B. & Rose, G.A. (2004). Homing and site fidelity in the greasy grouper Epinephelus tauvina (Serranidae) within a marine protected area in coastal Kenya. Marine Ecology Progress Series 277: 245-251.

Kaunda-Arara, B., Rose, G.A., Muchiri, M.S. & Kaka, R. [2003]. Long-term trends in coral reef fish yields and exploitation rates of commercial species from coastal Kenya. Western India Ocean Journal of Marine Science 2: 105-116.

Laurence, G.C. (1978). Length-weight relationships for seven species of northwest Atlantic fishes reared in the laboratory. Fishery Bulletin 76: 890-895.

Le Cren, E.D. (1951). The length-weight relationship and seasonal cycle in gonad weight and condition in the perch Perca fluviatilis . Journal of Animal Ecology 20 (2): 201-219.

Lee, Y.D., Park, S.H., Takemura, A. & Takano, K. (2002). Histological observations of seasonal reproductive and lunar-related spawning cycles in the female honeycomb grouper Epinephelus merra in Okinawan waters. Fisheries Science 68: 872–877.

Levin, P.S. & Grimes, C.B. (2002). Reef fish ecology and grouper conservation and management. in: P. Sale (Ed.) Coral Fishes Dynamics and Diversity in a Complex Ecosystem . Academic Press, San Diego, pp. 377–389.

Liu, M. & Sadovy, Y. (2004). The influence of social factors on adult sex change and juvenile sexual differentiation in a diandric, protogynous epinepheline, Cephalopholis boenak (Pisces, Serranidae). Journal of Zoology (London) 264: 239–248.

Mackie, M.C. (2003). Socially controlled sex-change in the half-moon grouper, Epinephelus rivulatus , at Ningaloo Reef, Western Australia. Coral Reefs 22: 133–142.

McClanahan, T.R. & Graham, N.A.J. (2005): Recovery trajectories of coral reef fish assemblages within Kenyan Marine protected areas. Marine Ecology Progress Series 294: 241-248.

McClanahan, T.R. (1988). Seasonality in East Africa’s coastal waters. Marine Ecology Progress Series 44: 191-199.

McClanahan, T.R., Graham, N.A., Calnan, J.M. & MacNeil, M.A. [2007]. Toward pristine biomass: reef fish recovery in coral reef marine protected areas in Kenya. Ecological Applications 17, 1055-1067.

McClanahan, T.R., Hicks, C.C., & Darling, E.J. (2008). Malthusian overfishing and efforts to overcome it on Kenyan coral reefs. Ecological Applications 18 (6): 1516-1529.

McIlwain, J., Hermosa, G.V., Claereboudt, M., Al-Oufi, H.S. & Al-Awi, M. (2006). Spawning and reproductive patterns of six exploited finfish species from the Arabian Sea, Sultanate of Oman. Journal of Applied Ichthyology 22: 167–176.

Millennium Ecosystem Assessment (MA), (2005). Ecosystems and human well-being: Policy Responses: Findings of the Responses Working Group of the Millennium Ecosystem Assessment. Washington D.C., Island Press.

Muchlisin, Z.A., Musman, M. & Azizah, M.N.S. (2010). Length-weight relationships and condition factors of two threatened fishes, Rasbora tawarensis and Poropuntius tawarensis, endemic to Lake Laut Tawar, Aceh Province, Indonesia. Journal of Applied Ichthyology 26(6): 949-953.

Munday P.L., Buston P.M. & Warner R.R. (2006). Diversity and flexibility of sex change strategies in animals. Trends in Ecology and Evolution 21: 89-95.

Myers, R.A., Baum, J.K., Shepherd, T.D, Powers, S.P. & Peterson, C.H. (2007). Cascading effects of the loss of apex predatory sharks from a coastal ocean. Science 315: 1846- 1849.

Nzioka, R.M. (1979): Observation on the spawning seasons of East African reef fishes. Journal of Fish Biology 14: 329-342.

Ochiewo, J. (2004). Changing fisheries practices and their socioeconomic implications in South Coast Kenya. Ocean & Coastal Management 10(3):120-127.

Pandolfi, M., Cánepa, M.M., Meijide, F.J., Alonso, F., Rey Vazquez, G., Maggese, M.C. & Vissio, P.G. (2009). Studies on the reproductive and developmental biology of cichlasoma dimerus (Perciformes, Cichlidae). Biocell 33 (1): 1-18.

Parker, G.A. (1990). Sperm competition games: raffles and roles. Proceedings:Biological Sciences 242: 120–126.

Patterson, W.F. III, Watterson, J.C., Shipp, R.L. & Cowen, J.H. Jr. (2001). Movement of tagged Red snapper in the northern Gulf of Mexico. Trans-Atlantic American Fishery Society 130: 533-545.

Pauly, D., Alder, J., Bakun, A., Heileman, S., Kock, K.H., Mace, P., Perrin, W., Stergiou, K., Sumaila, U.R., Vierros, M., Freire, S., Christensen, V., Kaschner, K., Palomares, M.L., Tyedmers, P., Wabnitz, C., Watson, R. & Worm B. (2005). Marine fisheries systems. In : R. Hassan, R. Scholes and N. Ash (Eds) Ecosystems and Human Well- being: Current State and Trends, Vol.1. Island Press, U.S.A., pp. 477-511.

Pears, R.J. (2009). Comparative demography and Assemblage structure of Serranid fishes: Implications for conservation and fisheries management. PhD Thesis. James Cook University, Australia.

Prasad, G. & Anvar, A.P.H. (2007). Length-weight relationship of a cyprinid fish Puntius filamentosus from Chalakudy River, Kerala. Zoos’ Print Journal 22 (3): 2637-2638.

Pullin, A.S., Knight, T.M., Stone, D.A. & Charman, K. (2004). Do conservation managers use scientific evidence to support their decision-making? Biological Conservation 119: 245-252.

Rahman, M.M., Hossain,M.Y., Hossain, M.A., Ahamed, F. & Ohtomi, J. (2012). Sex Ratio, Length-Frequency Distributions and Morphometric Relationships of Length- Length and Length-Weight for Spiny Eel, Macrognathus aculeatus in the Ganges River, NW Bangladesh. World Journal of Zoology 7 (4): 338-346.

Ramadan, A.M. & El-Halfawy, M.M. (2007). Common forms of Atresia in the ovary of some red sea fishes during reproductive cycle. Pakistan Journal of Biological Science 10: 3120-3125.

Rasotto, M.B. & Shapiro, D.Y. (1992). Protogynous sex change. in: R. Dallai(Ed.)Sex Origin andEvolution. Mucchi, Modena, pp. 379–389.

Rhodes, K.L. & Tupper, M.H. (2007). A preliminary market-based analysis of the Pohnpei, Micronesia grouper (Serranidae: Epinephelinae) fishery reveal unsustainable fishing practices. Coral Reefs 26: 335-344.

Rhodes, K.L. & Sadovy, Y. (2002). Temporal and spatial trends in spawning aggregation of the camouflage grouper, Epinephelus polyphekaidon, in Pohnpei, Micronesia. Environmental Biology of Fish 63: 27-39.

Robinson, J.M., Samoilys, M.A. & Kimani, P. (2008). Reef Fish Spawning Aggregations in the Western Indian Ocean: Current knowledge and implications for management.in: Obura, D.O., Tamelander, J. and Linden, O. (Eds.) Ten Years after bleaching: Facing the consequences of climate change in the Indian Ocean. CORDIO, Mombasa, Kenya. pp.: 263-276.

Sadovy de Mitcheson, Y. & Liu, M. (2008). Functional hermaphroditism in teleosts. Fish and Fisheries 9: 1–43.

Sadovy, Y.J. & Shapiro, D.Y. (1987). Criteria for the diagnosis of hermaphroditism in fishes. Copeia 1987: 136–156.

Sadovy, Y.J. (1996): Reproduction of reef fish. in: Polunin, N.V.C.; Roberts, C.M (Eds). Reef fisheries. Chapman and Hall. Fish and fisheries series pp.16-53.

Sale, P.F. (2002). Introduction . In : Sale, P.F. (Ed.). The ecology of fishes on coral reefs. Academic Press, San Diego, pp.3-25.

Sale, P.F. (2004). Connectivity, recruitment variation, and the structure of reef fish communities. Integrative and Comparative Biology 44: 390-399.

Samoilys, M.A. (1988). Abundance and species richness of coral reef fish on the Kenyan Coast: The effects of protective management and fishing. in: Proceedings of International Coral Reef Symposium 2: 261-266.

Sarkar U.K., Khan G.E., Dabas A., Pathak A.K., Mir J.I., Rebello S.C., Pal A. & Singh S.P. (2013). Length weight relationship and condition factor of selected freshwater species found in River Ganga, Gomti and Rapti India. Journal of Environmental biology 34: 951-956.

Sattar, A., Najeeb, A., Islam, F.A. & Wood, E. (2012). Management of the grouper fishery of the Maldives. Cairns, Australia.

Shapiro, D.Y. (1987). Reproduction in groupers. In : J.J. Polovina and S. Ralston (Eds). Tropical snappers and groupers: biology and fisheries management, West view Press, Boulder, Colorado, pp. 295-327.

Smith, M.M. & Heemstra, P.C. (1986). Smith’s Sea Fishes . Macmillan SA. Johannesburg, 1047 p.

Somers, K. (1991) Characterizing size-specific fecundity in crustaceans. In: Schram FR (ed) Crustacean egg production. Crust Issues 7. A.A. Balkema, Rotterdam, The Netherlands, pp 357–378.

Stewart, B.D. & Jones, G.P. (2001). Associations between the abundance of piscivorous fishes and their prey on coral reefs: Implications for prey-fish mortality. Marine Biology 138: 383-397.

UNEP-Nairobi Convention & WIOMSA (2015). The Regional State of the Coast Report: Western Indian Ocean. UNEP and WIOMSA, Nairobi, Kenya, 546 pp.

Wootton, R.J. (1991). Ecology of Teleost Fishes . Chapman and Hall, London.

WWF (2006): Living Planet Report 2006 . WWF-World Wildlife Fund for Nature (formerly World Wildlife Fund) Gland, Switzerland.

Zar, J.H. (2010). Biostatistical Analysis. 5th Edn. Prentice-Hall, Upper Saddle River, New Jersey, Englewood, USA. 662 pp.