impacts of pollution on the feeding, bioturbation and

53
Impacts of Pollution on the Feeding, Bioturbation and Biomass of the Fiddler Crab, Uca annulipes (H. Milne Edwards) in Gazi and Mikindani Mangroves, Kenya. By Owuor Margaret Awuor Reg.No: 156/13150/05 A thesis submitted in partial fulfilment of the requirements for the award of the degree of Master of Science (Fisheries Science) in the School of Pure and Applied Sciences of Kenyatta University November 2014

Upload: others

Post on 29-Oct-2021

4 views

Category:

Documents


0 download

TRANSCRIPT

Page 1: Impacts of Pollution on the Feeding, Bioturbation and

Impacts of Pollution on the Feeding, Bioturbation and Biomass of the Fiddler

Crab, Uca annulipes (H. Milne Edwards) in Gazi and Mikindani Mangroves,

Kenya.

By

Owuor Margaret Awuor

Reg.No: 156/13150/05

A thesis submitted in partial fulfilment of the requirements for the award of the degree

of Master of Science (Fisheries Science) in the School of Pure and Applied Sciences of

Kenyatta University

November 2014

Page 2: Impacts of Pollution on the Feeding, Bioturbation and

ii

DECLARATION

DECLARATION BY THE CANDITATE

Candidate

This thesis is my original work and has not been presented for the award of a degree in

any university or any other award.

Owuor Margaret Awuor

Signature…………………………. Date…………………..

DECLARATION BY SUPERVISORS

We confirm that the candidate carried out this work under our supervision.

Professor Peninna Aloo-Obudho

Karatina University

Signature…………………………. Date…………………..

Dr. Stefano Cannicci

Department of Evolutionary Biology

University of Firenze, Italy

Signature…………………………. Date…………………..

Dr. James Kairo Gitundu

Kenya Marine and Fisheries Research Institute

Mombasa, Kenya

Signature………… ………………. Date…………………..

Page 3: Impacts of Pollution on the Feeding, Bioturbation and

iii

DEDICATION

To my parents Joseph and Quinn Owuor for their support and encouragement.

To my late Grandmother Cecilia you were the rock of our family.

Page 4: Impacts of Pollution on the Feeding, Bioturbation and

iv

ACKNOWLEDGEMENTS

I gratefully acknowledge my supervisor Prof. Peninna Aloo-Obudho of Karatina University

formerly a lecturer at Kenyatta University for her guidance during the study. I am equally

grateful to my co-supervisors, Dr. James Kairo Gitundu of Kenya Marine and Fisheries

Research Institute (KMFRI) for giving me the opportunity to work in Gazi Field station,

and to Dr. Stefano Cannici of the University of Firenze, Italy for allowing me to join his

project team and providing me with necessary information on the project. Thanks to Dr.

Benson Mwangi for correcting and improving the final thesis.

Many thanks goes to Dr Johnson Kazungu, the Director of KMFRI for giving me the

opportunity to work in the laboratory, providing the necessary facilities and reagents.

I am sincerely indebted to the Peri-Urban Mangrove forests as Filters and Potential

Phytoremediators of domestic Sewage in East Africa (PUMPSEA) project for funding my

project. Many thanks to the Department of Zoological Sciences, for the partial Deans

scholarship which they awarded to me.

I take this opportunity to thank Prof. Callistus Ogol of Kenyatta University for his

unrelenting assistance both academically and administratively during my study at Kenyatta

University. Equally to Margaret Aloyo for her good managerial and administrative work at

the Department.

I wish to express my sincere gratitude to my laboratory colleagues and friends, Marco Fusi

and Filipo with whom we worked through the entire project. Extended thanks to PhD

student Benard Kirui, with whom we shared many ideas during study. Finally, compliments

to my classmate Margaret Kababu for accommodating me during part of my study, you are

so supportive.

To my family my loving husband and son (Joel), you have been very supportive both

morally and financially.

Page 5: Impacts of Pollution on the Feeding, Bioturbation and

v

TABLE OF CONTENTS

DECLARATION........................................................................................................... ii

DEDICATION.............................................................................................................. iii

ACKNOWLEDGEMENTS ........................................................................................ iv

TABLE OF CONTENTS ............................................................................................. v

LIST OF TABLES ...................................................................................................... vii

LIST OF FIGURES ................................................................................................... viii

ABBREVIATIONS AND ACRONYMS .................................................................... ix

ABSTRACT ................................................................................................................... x

CHAPTER 1: INTRODUCTION ................................................................................ 1

1.1 Background ............................................................................................................... 1

1.2 Problem statement and justification ................................................................. 4

1.3 Research Questions ................................................................................................... 5

1.4 Hypothesis................................................................................................................. 5

1.5. Objectives ................................................................................................................ 5

1.5.1. General objective ...................................................................................... 5

1.5.2. Specific objectives .................................................................................... 5

CHAPTER 2: LITERATURE REVIEW ................................................................... 6

2.1 Mangrove Ecosystem ................................................................................................ 6

2.2. Mangrove function and productivity ....................................................................... 8

2.3. Ecology and behavior of Fiddler crabs .................................................................. 10

2.3. Bioturbation activity of Fiddler crabs .................................................................... 12

2.3. Fiddler crab numbers and biomass ........................................................................ 14

CHAPTER 3: MATERIALS AND METHODS ...................................................... 15

3.1 Description of the study area .......................................................................... 15

3.2 Sampling design ............................................................................................. 19

Page 6: Impacts of Pollution on the Feeding, Bioturbation and

vi

3.3 Sampling methods .......................................................................................... 20

3.4 Observation Protocol ...................................................................................... 20

3.4.1. Chlorophyll a analysis ............................................................................ 22

3.4.2 Bioturbation ............................................................................................. 23

3.4.3 Crab biomass estimation .......................................................................... 24

3.5. Data Analysis ................................................................................................. 24

CHAPTER 4: RESULTS ........................................................................................... 25

4.1 Impacts of urban wastewater on the feeding rate of U. annulipes .......................... 25

4.2 Impacts of urban waste on the bioturbation activity of U. annulipes in human

impacted Mikindani and non-urban Gazi Bay. ............................................................. 26

4.3 Impact of pollution on Uca annulipes biomass ...................................................... 27

CHAPTER 5: DISCUSSION ..................................................................................... 31

CHAPTER 6: CONCLUSIONS AND RECOMMENDATIONS ........................... 34

6.1 CONCLUSIONS..................................................................................................... 34

6.2 RECOMMENDATIONS ........................................................................................ 35

REFERENCES ............................................................................................................ 36

Page 7: Impacts of Pollution on the Feeding, Bioturbation and

vii

LIST OF TABLES

TABLE 1: RESULTS OF THE FOUR FACTOR-ANOVA CONDUCTED ON SQUARE ROOTED

TRANSFORMED DRY WEIGHT (G) OF FEEDING PELLETS (USED TO FIND BIOTURBATION

DATA) RECORDED FROM MIKINDANI AND GAZI. .......................................................... 27

TABLE 2 : RESULTS OF THE FOUR FACTOR-ANOVA CONDUCTED ON SQUARE ROOTED

TRANSFORMED BIOMASS (EXPRESSED AS DRY WEIGHT (DW) DATA FROM

MIKINDANI AND GAZI .................................................................................................. 29

Page 8: Impacts of Pollution on the Feeding, Bioturbation and

viii

LIST OF FIGURES

FIGURE 1: MANGROVES AERIAL ROOTS. DOTTED LINES REPRESENT SOIL LEVELS (FROM

SHUNULA AND WHITTICK, 1996). ........................................................................... 7

FIGURE 2: MANGROVE SEEDS OF (1) RHIZOPHORA MUCRONATA, (2) BRUGUIERA

GYMNORHIZA, (3) BRUGUIERA PARVIFLORA, (4) AVICENNIA MARINA (A) NEWLY

GERMINATED, (B) SHOOTING, (5) AEGICERAS CORNICULATA (A) BUNCH OF FRUITS,

(B) YOUNG FRUIT AND (C) GERMINATING FRUIT (MACNAE 1968) ........................... 8

FIGURE 3: IMAGE OF FIDDLER CRAB UCA ANNULIPES BURROWS IN OPEN FIELD, GAZI BAY ... 13

FIGURE 4: POLLUTANTS DRAINING TO THE MANGROVES FROM RESIDENTIAL AREAS IN

MIKINDANI (PHOTOS BY CHARLES MITTO)............................................................ 17

FIGURE 5: MAP SHOWING THE STUDY AREAS IN TUDOR CREEK AND GAZI BAY ALONG THE

KENYA COAST ....................................................................................................... 18

FIGURE 6: FORESTED (AVICENNIA MARINA ZONE) AND OPEN AREA (DESERT ZONE) (PHOTO

BY FILIPO) .............................................................................................................. 19

FIGURE 7: PHOTO SHOWING QUADRATS SET IN THE A MARINA AND DESERT ZONES (PHOTOS

BY MARCO) ........................................................................................................... 21

FIGURE 8: SAMPLING DESIGN INDICATING THE SAMPLING ZONES AND TRANSECTS .............. 22

FIGURE 9: MEAN ( x ± SE) CHLOROPHYLL A CONCENTRATION IN THE PROCESSED AND

NON-PROCESSED SEDIMENTS (SOIL) IN GAZI AND MIKINDANI WITHIN THE

AVICENNIA MARINA AND DESERT ZONES ................................................................ 25

FIGURE 10: MEAN ( x ± SE) DRY WEIGHTS (G) OF FEEDING PELLETS COLLECTED IN

MIKINDANI AND GAZI WITHIN THE AVICENNIA MARINA AND DESERT ZONE ........... 26

FIGURE 11: MEAN ( x ± SE) DRY WEIGHTS (G) OF UCA ANNULIPES (BIOMASS) COLLECTED

IN MIKINDANI AND GAZI WITHIN THE AVICENNIA MARINA AND DESERT ZONE ....... 28

FIGURE 12: THE DRY WEIGHT OF BIOTURBATED MATERIAL IN RELATION TO FIDDLER CRAB

U. ANNULIPES BIOMASS .......................................................................................... 30

Page 9: Impacts of Pollution on the Feeding, Bioturbation and

ix

ABBREVIATIONS AND ACRONYMS

ANOVA Analysis of Variance

BOD Biological Oxygen Demand

CL Carapace Length

CW Carapace Width

DW Dry Weight

FAO Food and Agriculture Organization

GESAMP Group of Experts on the Scientific Aspects of Marine Pollution

GoK Government of Kenya

GPA Global Programme of Action

ICLARM International Centre for Living Aquatic Resources Management

KMFRI Kenya Marine and Fisheries Research Institute

PUMPSEA Peri-urban Mangroves forests as filters and Potential

phytoremediators of domestic Sewage in East Africa

UNEP United Nations Environment Programme

Page 10: Impacts of Pollution on the Feeding, Bioturbation and

x

ABSTRACT

Marine pollution is one of the main anthropogenic factors identified globally to affect the

estuarine and coastal ecosystems. One of the recipients of pollutants is the mangroves since

they are intercepting between land and ocean. In recent years, the mangrove forests have been

proposed for use as natural wastewater treatment wetlands. This is based on research findings

conducted in countries like China. However, before promoting the use of natural mangrove as

pollution buffers, the effect of these pollutants on the ecosystems‟ biodiversity must be

assessed. This study aimed at determining the impact of pollution on the feeding, bioturbation

and biomass of the fiddler crab Uca annulipes in Gazi and Mikindani along the Kenya Coast.

The mangroves in Mikindani on Tudor creek represented peri-urban mangroves which are

heavily impacted by municipal wastewater, while the mangroves in Gazi Bay in the South

Coast of Kenya represented mangroves not affected by direct sewage input. In addition, crabs

Uca annulipes are one of the most important groups of mangrove epifauna. To investigate the

impacts of pollution on the feeding, bioturbation and biomass of Uca annulipes a stratified

nested design was adopted. The mangroves selected for the study manifested distinctive

zonation pattern in the dominance of their mangrove species, due to this, a stratified random

sampling approach was applied at each site. Sampling was conducted in 2 × 2 m2 quadrats in

desert and Avicennia zones during July, August and October 2005. Data collection depended on

each full moon springs and new moon springs when spring tides would be realised. Different

parameters were measured, Chlorophyl a (Chl a) concentrations in the feeding pellets and non-

processed soils, amount of bioturbated soils (expressed as dry weight of excavated material and

feeding pellets), and biomass (dry weight) of Uca annulipes. Four factor Analysis of Variance

(ANOVA) tests were applied to determine whether there were significant difference in feeding,

bioturbation and biomass of Uca annulipes within the two sites. Results show significant

differences in Chl a concentration was observed in the feeding pellets in the Avicennia zone

(F1, 88=0.146; p < 0.05) of the peri-urban mangroves. Moreover Chl a concentration did not

vary between the processed (0.36 ± 0.07) and non-processed soils (0.32 ± 0.07) in the

Avicennia zone. In Gazi Significant difference in bioturbated material was recorded compared

to Mikindani (F1, 16=70.65; p < 0.05). ). The results manifested a consistent increase in crab

biomass at the peri-urban site, than the non urban mangroves (F1,16=75.28, p>0.05).The

Avicennia zone of the peri-urban site had a higher Uca annulipes biomass compared to the non-

urban Gazi (F1,16=54.48, p<0.05). There was no relationship between the mass of bioturbated

material and Uca biomass (R2

=0.0197, p < 0.05). Results also show that the amount of

excavated material did not relate to the Uca biomass (R2 = 0.0248, p < 0.05). In conclusion,

fiddler crabs through feeding, burrowing and ventilation activities have an influence on

microbial activity and sediment metabolism in marine sediments. Therefore, the feeding pattern

in the peri-urban site indicated the need for further study of the actual potential of natural

mangroves to absorb pollutants in sewage water since it will be important to find out what the

crabs are feeding on.

Page 11: Impacts of Pollution on the Feeding, Bioturbation and

1

CHAPTER 1: INTRODUCTION

1.1 Background

The importance of marine resources is known worldwide and so cannot be ignored. Coastal

biodiversity i.e. crabs, fish play an important role in supporting the livelihood of the many

coastal communities through among others fisheries. More than one third of the world‟s

population live in the coastal zone (UNEP, 2006). The coastal zone is a narrow strip

constituting 4 % of the total land surface (UNEP, 2006; Okuku et al., 2011). However, rapid

increase in population, food production, urbanization and coastal development in most of the

world‟s coastal regions are causing serious environmental concerns such as marine pollution

(Seitzinger et al., 2005). Different kinds of marine pollutants have been identified, these

include, oil, sewage, garbage, chemicals, radioactive waste and thermal pollution (Clark et

al., 2001).

Studies show that 80 % of marine pollution originates from land-based sources that reach

estuaries and coastal waters via non-point runoff, direct deposit of waste and atmospheric

fallout (GESAMP, 1990; Vijay et al., 2008). Despite the significant contribution of land-

based activities to coastal pollution, it has not been given adequate attention (UNEP, 2006).

Most eutrophication and organic loading problems in coastal regions in the world are linked

to discharge of sewage effluent and dumping of sewage sludge (Subramanian, 1999). Coastal

ecosystems have been found to act as receptors for industrial and municipal effluents

(Palanisamy et al., 2007).

Sewage can be defined as a cocktail of waste from food preparation, dishwashing, garbage-

grinding, toilets, baths, showers and sinks (Okuku et al., 2011). It contains a wide variety of

dissolved and suspended materials as well as disease-causing microorganisms. Densely

Page 12: Impacts of Pollution on the Feeding, Bioturbation and

2

populated communities generate such large quantities of sewage that dilution by ocean waters

alone cannot avert pollution incidences.

Sewage pollution has been identified as one of the most serious of all land based threats to

the marine environment (UNEP, 2006). 80-90 % of sewage is discharged in to the coastal

zones of many developing countries untreated (UNEP, 2006). This puts the human and

wildlife (Jenssen, 2003) as well as livelihoods (fisheries to tourism) at risk through reduction

of biodiversity and productivity (Hunter and Evans, 1995), and the aesthetic and intrinsic

value of the marine environment especially when sewage discharge occurs into relatively

shallow and sheltered coastal areas like the mangrove systems as in the case of Kenya

(Okuku et al., 2011).

In the Kenya, the coastal town of Mombasa is reported to face serious challenges of sewage

pollution. Mombasa city has only one sewage treatment facility which had previously stalled

for several years and is currently working at 50 % capacity after renovation (Okuku et al.,

2011). This 50 % capacity can barely serve even 12 % of the Mombasa city population

leading to volumes of sewage being discharged either untreated or slightly treated (Okuku et

al., 2011).

The mangrove ecosystem is one of the coastal ecosystems under the influence of sewage

discharge. Peri- urban mangroves of Mombasa are recipients of sewage-polluted rivers and

flash-flood waters and are used for sewage dumping, with possible risk to human health,

fisheries and ecosystems (De Wolf et al., 2000). Studies have been carried out in countries

like China (Cannicci et al., 2008) which indicate that mangrove swamps have potential for

use as natural wastewater treatment areas (Wong et al., 1995). Mangrove sediments have

been found to be efficient in absorbing nutrients, mainly phosphorus and nitrogen from

sewage (Tam and Wong, 1995), and shrimp farming wastes (Trott et al., 2004). However,

Page 13: Impacts of Pollution on the Feeding, Bioturbation and

3

literature on the effects of sewage and peri-urban effluents on the faunal component of

shallow water ecosystems is not encouraging (Cannicci et al., 2008).

Faunal assemblages in the mangroves have been found to vary spatially, this brings

confounding factors in the results (Chapman and Tolhurst, 2004). Microfaunal distributions

and diversity in peri-urban coastal systems have been found to be susceptible to a variety of

pollutants and impacts, such as metals (Bergey and Weiss, 2008), pesticides (Garmouma et

al., 1998), hydrocarbons (Inglis and Kross, 2000). Fiddler crabs have been reported to be one

group of organisms that are exposed to pollution being strict residents of mangroves

throughout their adult life (Skov et al., 2002; Fratini et al., 2004) that ingest sediment

(Cannicci et al., 2008).

The present study was carried out based on the background of concerns that sewage disposal

could result on diversity loss of Fiddler crab Uca annulipes. The study was designed to

investigate the impact of pollution on the feeding, bioturbation and the biomass of fiddler

crab Uca annulipes between peri-urban mangroves (Mikindani), impacted by sewage

disposal and non-urban sites with no evident sewage disposal (Gazi Mangroves). The status

of coastal ecosystems is an important indicator of environmental quality in terms of pollution

load and related issues. The information collected from these study aspects will highlight the

need for urgent planning and action in the areas studied.

Page 14: Impacts of Pollution on the Feeding, Bioturbation and

4

1.2 Problem statement and justification

Sewage pollution is one of the main problems facing the mangrove ecosystem along the

Kenya coast. This is heightened by the reported increase in population and, the limited

provision of sewage treatment facilities by the local authorities. The repercussion of the

sewage discharge is death or loss of biodiversity causing changes in the mangrove ecosystem.

Mangroves act as buffers along the coastline and within the mangrove ecosystem organisms

live according to the zonation of the ecosystem from landward covered by the Avicennia

marina to the seaward. Therefore, anthropogenic factors causing interference with the

biodiversity of one zone could also interfere with other zones. The mangrove ecosystem is a

home to a number of organisms i.e. crabs, birds, fish, all these organisms depend on each

other based on the trophic levels. Therefore disappearance of one species could result in the

loss of those that depend on them for example birds feed on crabs, fish. One of the organisms

influenced by the nourishment from nutrients introduced by the sewage discharge is the

fiddler crab Uca annulipes, this is because they feed on the sediments benthic microalgae and

bacteria. They benefit from organic matter deposited on the sediment surface under enriched

situations and are thus good indicators of habitat disruption.

Fiddler crabs also play an important role in the mangrove ecosystem through their

bioturbation and feeding activity where they roll and move the sediments hence causing

aeration. They are referred to as coastal engineers. Therefore, the above study investigated

the impact of sewage pollution on the feeding and bioturbation activities of the fiddler crab,

Uca annulipes in an attempt to find out the impacts of pollution on the mangrove ecosystem.

The study also compared the biomass of Uca annulipes in peri urban site Mikindani and non-

urban mangrove systems of Gazi.

Page 15: Impacts of Pollution on the Feeding, Bioturbation and

5

1.3 Research Questions

1. How does the feeding rate of Uca annulipes vary between human impacted mangroves of

Mikindani and those in pristine Gazi?

2. Is there a difference in the rate of bioturbation of Uca annulipes in human impacted

mangroves of Mikindani and those of pristine Gazi?

3. How does the biomass of Uca annulipes differ between the human impacted Mikindani

mangroves and the pristine Gazi?

1.4 Hypothesis

There is no difference in the feeding, bioturbation and biomass of Uca annulipes in human

impacted mangroves of Mikindani and those in pristine Gazi.

1.5. Objectives

1.5.1. General objective

To investigate the impacts of sewage discharge on the feeding rate, bioturbation and biomass

of Uca annulipes in mangrove forests of peri-urban impacted mangroves of Mikindani and

non-urban mangroves of Gazi Bay.

1.5.2. Specific objectives

1. To determine the feeding rate of Uca annulipes in human impacted mangroves of

Mikindani and in pristine Gazi.

2. To evaluate the variation in the rate of bioturbation of U. annulipes in Mikindani and

Gazi.

3. To determine if there were any significant differences in the biomass of Uca annulipes

between human impacted mangroves of Mikindani and non-impacted Gazi.

Page 16: Impacts of Pollution on the Feeding, Bioturbation and

6

CHAPTER 2: LITERATURE REVIEW

2.1 Mangrove Ecosystem

The word „mangrove‟ has two meanings: it can refer to the trees, or the mangrove ecosystem.

An in-depth description of mangroves and their habitat is beyond the scope of the present

study. However, different authors have given general descriptions which we can refer to and

which the following study was based on (Chapman, 1944; MacNae, 1968; Lugo and

Snedaker, 1974; Odum et al., 1985; Por and Dor, 1984; Tomlinson, 1986; Hartnoll, 1988;

Shunula and Whittick, 1996; Hogarth, 1999; Kathiresan and Bingham, 2001).

Mangrove trees colonise the interface between land and sea in the tropics and subtropics.

Between 54 (Tomlinson, 1986) and 69 (Duke, 1992) mangrove species are recognised

depending on definition. All mangrove species are flowering, seed producing plants

(dicotyledons), with the exception of the palm Nypa (Duke, 1992). Trees have the ability to

grow in saline conditions. This does not mean they require salt water (Skov et al., 2002). On

the contrary, many species prefer terrestrial environments, but their slow growth leaves them

outcompeted in areas without saline influence (Tomlinson, 1986).

Terrestrial species with a degree of salt acceptance frequently coexist with true mangrove

species in the terrestrial fringe. Ecologists consequently divide mangrove trees into true

„mangroves‟, „minor mangrove species‟ and „mangrove associates‟ (Tomlinson, 1986). The

exact classification varies between ecologists, but in general true mangroves are characterised

by:

Occurring only in mangrove swamps

Frequently forming single-species forests (stands)

Having „special structures‟ for adaptation to their environment

Page 17: Impacts of Pollution on the Feeding, Bioturbation and

7

Having physiological adaptations to deal with saline conditions

Being taxonomically isolated from terrestrial relatives, at least at generic level

Mangrove „special structures‟ include: (1) aerial roots (e.g. „pneumatophores‟. See fig. 1),

which allow gas exchange in often anoxic mud (Scholander et al., 1955), (2) prop roots,

which prevent trees from falling over in soft mud and currents (Fig. 1) and (3) viviparity

(production of seeds that germinate whilst still within the fruit). Seeds (Fig. 2) vary between

families and range from cherry-sized, fruit-like, semi-viviparous spheres (e.g. Avicennia sp.),

to ~30 cm long, cigar-shaped, truly viviparous „hypocotyls‟ (e.g. Rhizophora. sp.).

Physiological adaptations to saline conditions include mechanisms for reducing salt uptake

by roots and various mechanisms for salt excretion (e.g. salt glands in the leaves of

Avicennia).

Figure 1: Mangroves aerial roots. Dotted lines represent soil levels (from Shunula and Whittick,

1996).

Page 18: Impacts of Pollution on the Feeding, Bioturbation and

8

Figure 2: Mangrove seeds of (1) Rhizophora mucronata, (2) Bruguiera gymnorhiza, (3)

Bruguiera parviflora, (4) Avicennia marina (a) newly germinated, (b) shooting, (5) Aegiceras

corniculata (a) bunch of fruits, (b) young fruit and (c) germinating fruit (MacNae, 1968)

2.2. Mangrove function and productivity

Mangroves perform a number of ecosystem functions and services (Duke et al., 2007). The

rate of primary production in this ecosystem is one of the highest of any ecosystem (>2 t ha-1

yr-1

). As a result, they play a key role in nutrient cycling in coastal ecosystems and global

carbon cycling. Therefore, mangrove forests have been demonstrated to act both as nutrient

sources and sinks (Kristensen et al., 2008). Carbon cycling and other ecosystem processes in

mangroves provide crucial ecosystem services to estuarine habitats such as nursery areas for

fish, prawns and crabs (Nagelkerken et al., 2008).

Coastal human communities that live near mangrove areas also rely on them for provision of

a variety of food, timber, tannins and medicines derived from mangrove forests (Glaser,

2003; Walters et al., 2008). Mangroves are also important in coastal protection, this

Page 19: Impacts of Pollution on the Feeding, Bioturbation and

9

ecological function was demonstrated in the 2004 tsunami when mangroves in good

ecological condition proved effective (Dahdouh-Guebas et al., 2005). In addition, mangroves

host a unique set of associated fauna, such as semi-terrestrial and tree-dwelling brachyuran

crabs (Fratini et al., 2005; Cannicci et al., 2008) and insects (Cannicci et al., 2008), and,

within soft-sediment habitats, they provide a unique hard-sediment substratum needed for a

unique and diverse assemblage of benthos (Farnsworth and Ellison, 1996).

Apart from the above main ecological services offered by mangroves to the society,

mangroves have been found to be able to work as wastewater treatment areas, (Clough et al.,

1983; Wong et al., 1995, 1997). Studies have reported that mangroves intercept land-derived

pollutants hence limiting their dispersal offshore (Rivera-Monroy and Twilley, 1996).

Wolanski (2000) reported that mangroves may prevent estuarine eutrophication by

intercepting the release of prawn farm effluents. Mangroves are also very efficient in

absorbing nutrients, mainly phosphorous and nitrogen, derived from sewage (Tam and Wong,

1996), and shrimp farming effluent (Trott et al., 2004).

In a field trial of two years carried out in the Funtian Mangrove which are planted fields

(Wong et al., 1997) found that sewage disposal had no harmful effect on the higher plant

communities. Yu et al. (1997) detected no significant effects of wastewater on benthic

biomass, density and community structure at the same experimental site. However, they

measured a significant decrease in the diversity and biomass of gastropods. Despite the

evidence shown by studies from the Funtian mangroves in China that the mangrove

ecosystem are tolerant to sewage pollution, it is important for studies to be carried out on the

need to use natural mangrove sites for sewage disposal (Cannicci et al., 2009). Kathiresan

and Bingham (2001) suggested that the results obtained at Funtial mangrove (Cannicci et al.,

2009) may not be applicable to other sites, since Indo-Pacific mangrove forests (Kenya

Page 20: Impacts of Pollution on the Feeding, Bioturbation and

10

mangroves being one of these), differ widely and their unique characteristics may lead to

differences in tolerance to pollution.

Pollutants such as nutrients and biodegradable organic matter are generated in large amounts

by estuarine settlements, agriculture and aquaculture (Lee, 1998). These contain organic

matter, nutrients, and microorganisms, including pathogens, heavy metals and suspended

solids. Therefore, there is need for caution to be taken so that effects of organic loading do

not affect the enormous role in the ecosystem of mangroves such as nursery grounds and

source of resources for the coastal communities (Hogarth, 2007).

2.3. Ecology and behavior of Fiddler crabs

The mangrove environment supports a number of fauna that are an important integral

component of the ecosystem. Mangrove fauna serve in determining the structure and

functioning of its ecosystem as a whole (Lee, 1998; Bosire et al., 2004). The macrobenthic

faunal composition in mangrove forests is diverse and crabs are among the most prominent

species (Ruwa, 1997). Crabs are generally the key structuring faunal group and the driver of

the decomposer food webs in mangrove forest (Lee, 1998). Within the mangroves, there

exists a distinct faunal zonation based on mangrove forests zonation and on the shore levels

(Ruwa, 1997). The Avicennia marina zone is characterized by the presence of Sesarma

meinerti, Sesarma eulimeni, Sesarma ortmanni, Uca inversa, Uca lactea annulipes and

Cardisoma carnifex. These crabs are also found in the higher shore levels (Ruwa, 1997). The

detritivorous crabs that break down litter in the mangrove environment are species of the

genera Sesarma and Cardisoma. Species of Uca and Macrophthalmus usually extract their

food from sediments while the portunid crab, Scylla serrata, is a scavenger (Micheli et al.,

1991).

Page 21: Impacts of Pollution on the Feeding, Bioturbation and

11

Fiddler crabs (Genus: Uca, Family: Ocypodidae) are one of the most important groups of

brachyuran crabs in subtropical and tropical regions in terms of diversity and density

(Olafsson and Ndaro, 1997; Hartnoll et al., 2002). They are one of the most conspicuous

groups of bioturbating animals in mangrove forests (Nielsen et al., 2003), due to their

colourful appearance and often high density on the sediment surface. They have been shown

to dramatically alter the environment in which they live (Robertson, 1980; Dye and Lasiak,

1987). Fiddler crabs (Ocypodidae) are deposit- feeders, and are efficient consumers of

benthic microalgae (Reinsel, 2004). Foraging by fiddler crabs affect sediment organic

content, density of microalgae (measured as Chlorophyll a, hereafter Chl a), and taxonomic

composition of the meiofauna (Reinsel, 2004). Ocypodids like grapsid crabs are known to

actively feed from organic enrichment by exploiting the large amount of organic matter

deposited on the sediment surface under enriched conditions (Lee, 1998). This can result in

bioaccumulation of toxic substances posing serious harm to species at higher levels of

biological organization which prey on these crabs like fishes, birds and large benthic

invertebrates, and in turn cause serious public health problems to people who harvest these

organisms commercially or for recreational purpose (Bilyard, 1987).

Six species of Uca have been recorded in the Western Indian Ocean. In Eastern Africa

region, these are Uca annulipes (H. Milne Edwards), Uca gaimardi (H. Milne Edwards), Uca

inversa inversa (Hoffman) and Uca urvillei (H. Milne Edwards) (Skov and Hartnoll, 2001).

Of these Uca annulipes is arguably the most abundant (Hartnoll et al., 2002). It occupies a

range of substrates and forms a significant component of East African mangrove brachyuran

(Icely and Jones, 1975; Hartnoll et al., 2002). Like other deposit feeders, Uca. annulipes

dwells in burrows, which it digs to a depth of up to 0.5 m depending on shore level (Skov et

al., 2002). This species is diurnally active, emerging as the tide recedes (Macia et al., 2001).

Their surface activity terminates when burrows are re entered and plugged.

Page 22: Impacts of Pollution on the Feeding, Bioturbation and

12

Globally, different studies have been done to investigate the impact of different contaminants

on the behavioural activities of Fiddler crabs. Culbertson et al. (2007) reported on the long-

term biological effect of petroleum residues on fiddler crabs in salt marshes. Studies on the

feeding activities of fiddler crabs include among others, Georgia (Robertson et al., 1980),

Portugal (Wolfrath, 1992), North Carolina (O‟lafsson and Ndaro, 1997). In Kenya, most

studies on mangroves have so far tended to concentrate on distribution, utilization,

community composition and zonation of the mangrove species (Kokwaro, 1985; Abuodha

and Kairo, 2001). Studies on macrofauna have been undertaken by Fondo and Martens

(1998) who investigated the effects of mangrove deforestation on macrofaunal densities in

Gazi bay. Bosire et al. (2004) looked at spatial variations in macrobenthic fauna

recolonisation in a tropical mangrove bay while studies on feeding of crabs have focused on

Grapsids; (Dahdouh-Guebas et al., 1999). Studies on Uca crab have been carried out by Icely

and Jones (1975), who looked at factors affecting the distribution of Uca along the East

African shore. Little information exists on the status of peri-urban mangroves globally, and

few studies have been carried out on the effect of urban wastewaters on the feeding,

bioturbation and biomass of mangrove biodiversity for example Uca crabs.

2.3. Bioturbation activity of Fiddler crabs

The benthic fauna in mangrove forests is usually dominated by burrowing sesarmids

(Grapsidae) and fiddler craps (Ocypodidae). The two groups are herbivores that retain, bury,

macerate and ingest litter and microalgal mats (Kristensen, 2008). Most species within these

two groups actively dig and maintain burrows in the sediment as refuge from predation and

environmental extremes (Kristensen, 2008). Based on the knowledge on biology and ecology

of these crabs, it is obvious that their activities have considerable impact on the ecosystem

functioning. The burrows affect sediment topography and biogeochemistry by modifying

Page 23: Impacts of Pollution on the Feeding, Bioturbation and

13

particle size distribution, drainage, redox conditions and organic matter as well as nutrient

availability (Botto and Iribarne, 2000).

Fiddler crabs prefer to make burrows in open areas as in the Avicennia marina zones,

particularly near creek banks, this is where it has been found that strong sunlight stimulates

growth of microphytobenthos which are the primary food source for the fiddler crabs (

Nobbs, 2003). Studies show that the morphology of fiddler crab burrows is quite simple and

similar among species, the burrows are more or less permanent vertical shaft extending 10 to

40 cm into the sediment (Kristensen, 2008). The fiddler crabs continuously construct,

maintain and abandon their burrows. The amount of sediment excavated during burrow

construction and maintenance is considerable (Kristensen, 2008). McCaith et al. (2003) in a

study carried out in North American salt marsh estimated that populations of Uca pugnax can

construct between 40 to 300 burrows per meter square and through this excavate 120 to 160

cm/square of sediment. The study by McCaith also reported that when the Uca pugnax

excavated they mixed the upper 8 to 15 cm of the sediment.

As a result, fiddler crabs alter the quality of organic matter on the sediment surface by

replacing surface derived reactive material (e.g. fresh microphytobenthos) with much less

reactive and partly degraded material from depth in the sediment (Gutiérrez et al., 2006)

Figure 3: image of Fiddler crab Uca annulipes burrows in open field, Gazi bay

Page 24: Impacts of Pollution on the Feeding, Bioturbation and

14

2.3. Fiddler crab numbers and biomass

Brachyuran crabs are among the most important taxa (Macia et al., 2001), this is with regards

to their number of species, density and total biomass (Macia et al., 2001; Skov et al., 2002).

The most common of the mangrove crabs are the fiddler crabs (Family Ocypodidae, genus

Uca) or sesarmid crabs (Family Grapsidae, subfamily Sesarminae) (Hartnoll et al., 2002).

Studies carried out on Density and biomass estimates of fiddler crabs are very few of fiddler

crabs are (Icely and Jones, 1978), making it difficult to evaluate the relative importance of

fiddlers. Lee (1998) remarked in his review that „one area of uncertainty in the overall

importance of the crabs arises from the lack of a satisfactory method for the estimation of

field density‟

Despite the above mentioned problem, different researchers have come up with different

methods to estimate the population densities of crabs inhabiting mangroves (Nobbs &

Mcguinness, 1999; Macia et al., 2001). It is important to mention in this study that due to the

crab Uca annulipes habit of emerging from burrows during ebb tide, population size can be

estimated using a variety of methodologies (Macia et al., 2001; Litulo, 2005). Macia et al.

(2001), shows that absolute estimates can be produced through direct excavation of crabs

from their burrows, while direct visual counts can be made of surface-active animals, or of

their burrows (Skov et al., 2002). The methods used in the estimation of crabs‟ population

involve uncertainties (Skov and Hartnoll, 2001).

Page 25: Impacts of Pollution on the Feeding, Bioturbation and

15

CHAPTER 3: MATERIALS AND METHODS

3.1 Description of the study area

In the tropics most of the cities are built around natural harbours or waterways that are lined

by mangrove swamps (PUMPSEA, 2007). In Africa, such cities include Mombasa, (Kenya),

Dar-es-Salaam, (Tanzania) and Maputo (Mozambique) (De Wolf et al., 2000). Peri-urban

mangroves of these cities are recipients of sewage-polluted rivers and flash-flood waters and

are extensively used for sewage dumping.

This study was carried out along the Kenyan coast in two geographically different sites; Gazi

Bay and Mikindani on Tudor creek (Fig. 5). Gazi Bay is located at the South coast of Kenya,

47 km South of Mombasa (039.300o E, 04.220

o S), in Kwale county. The Bay is sheltered

from strong waves by the presence of Chale Peninsula to the East and fringing coral reefs to

the South. The upper region of the Bay is drained by Kidogoweni River, while south-western

region of the Bay is drained by the Mkurumuji River. Their combined freshwater discharge is

17.ms3-1

and is the main sources of dissolved inorganic nutrients (Kitheka, 1996; Kitheka et

al., 1996). The mangrove species commonly found in this area include Avicenna marina

(Forsks), Bruguiera gymnorhiza (Lam), Ceriops tagal (Robinson), Lumnitzera racemosa

(Willd), Rhizophora mucronata (Lam), Sonneratia alba (Smith) and Xylocarpus granatum

(Koen).

Mikindani on the other hand is a mangrove system located within Tudor Creek, which

surrounds the city of Mombasa. Mombasa which is a peri-urban island area is surrounded by

two main creeks namely, Tudor and Port Reitz. It has a population of 917,864, an average

population density of 3,111 persons per km2

and an annual growth rate of 3.6% (GoK, 2005).

The mangroves of this area have been faced with serious anthropogenic challenges. In the

Page 26: Impacts of Pollution on the Feeding, Bioturbation and

16

years 1893 to 1993, the port of Mombasa and its adjacent waters experienced five tanker

accidents spilling a total of 391,680 tonnes of oil (Abuodha and Kairo, 2001). A major spill

in 1988 destroyed 10 ha of mangroves in Makupa (Abuodha and Kairo, 2001; FAO, 2005),

and in 2005, 200 tons of crude oil were spilled, affecting 234 ha of mangroves in Port Reitz

creek (Kairo et al., 2005). In addition, the Mombasa municipal waste contributes about 4369

ton/year of biological oxygen demand (BOD), 3964 ton/year of suspended solids, 622

ton/year of nitrates and 94 ton/year of phosphates into the creeks in the form of raw sewage

(Mwaguni and Munga, 1997). This is in addition to coliform and Escherichia coli levels of

1800+ per 100 ml and up to 550 cfu per 100 ml respectively (Mwaguni and Munga, 1997).

The sewage runs through the mangrove forest in canals, first affecting the forest ecosystem

dominated by A. marina, before flowing towards the sea in an ecosystem dominated by R.

mucronata and finally reach Tudor Creek (fig. 4). Mangroves in this creek are flooded by

sewage in every tidal cycle. However, studies show that the load reduces exponentially with

distance from source (Kitheka et al., 2003; Mohamed, 2008; Mohamed et al., 2008). About

1200 kg of nitrogen and 5.5 kg of phosphorous are discharged via sewage into the Mikindani

system every day (Mohamed et al., 2008). Although this site is dominated by A. marina and

R. mucronata (a typical feature of Kenyan mangrove forests), all other East African

mangrove species are present, with the exception of Heritiera littoralis and Pemphis acidula.

Page 27: Impacts of Pollution on the Feeding, Bioturbation and

17

Figure 4: Pollutants draining to the mangroves from residential areas in Mikindani (photos by Charles

Mitto)

Page 28: Impacts of Pollution on the Feeding, Bioturbation and

18

Figure 5: Map showing the study areas in Tudor creek and Gazi bay along the Kenya coast

Page 29: Impacts of Pollution on the Feeding, Bioturbation and

19

3.2 Sampling design

To investigate the impacts of pollution on the feeding, bioturbation and biomass of fiddler

crab Uca annulipes a stratified nested design as described by Underwood (1992, 1994) was

adopted. The mangroves selected for the study manifested distinctive zonation pattern in the

dominance of their mangrove species maintained by associated faunal assemblages (Skov et

al., 2002). Due to this distinctive zonation, a stratified random sampling approach was

applied at each site. Two belts of the Avicennia marina were considered, that is the landward

sandy belt dominated by Avicennia marina (here referred to as the A marina zone)

representing the zone flooded only during spring tides and open area (here referred to as

desert zone- an area without any mangrove trees) flooded twice a day during high tides (fig.

6). Uca annulipes also dominates the Avicennia marina zone. They live in burrow in the

forested area during the high tides, but during low tides they come out to feed in the desert

zone.

Figure 6: Forested (Avicennia marina zone) and open area (desert zone) (Photo by Filipo)

Avicennia marina

zone

Desert zone

Page 30: Impacts of Pollution on the Feeding, Bioturbation and

20

3.3 Sampling methods

Sampling was carried out after spring tides receded and intertidal flats became exposed. Two

random transects (100-500m apart) were selected in each of the two zones (A. marina and

Desert) in both, Mikindani and Gazi. In each transect, three 2 by 2 m quadrats were set and

randomly sampled to assess the feeding and bioturbation activity of the fiddler crabs. At the

peri-urban sites, care was taken to locate transects close to the sewage dumping channels to

obtain data on areas directly affected by the wastewaters. The study was carried out during

July, August and October 2005. Data collection depended on each full moon springs and

again on the following new moon springs when spring tides would be realised. The factor

“Time” was very important since we had to wait for spring tides, inundation of the study sites

depended on these factors. As mentioned earlier crab activity also depended much on tidal

effect. The total work period at each location was spread over six weeks (except where it was

possible to work the two sites on the same tidal cycles): Full moon springs 1, Site 1 (Gazi);

New moon springs 1, Site 1; Full moon springs 2, Site 2 (Mikindani); New moon springs 2,

Site 2.

3.4 Observation Protocol

Observations were made in the two transects, guide ropes were position before observation.

In each transect, three 2 by 2 m quadrats were set and randomly sampled (Fig. 8). Surface

activity (feeding and bioturbation) was evaluated twice for each quadrat, one hour after

emersion in water during the spring high tides, and at low water. Observers were positioned

3 -4 m from the quadrats, there was a wait for 15 minutes to allow normal activity of the

crabs to resume. These times were found to be adequate. After the observational time was

over different activities took place, (i) soil samples were collected both from the feeding

Page 31: Impacts of Pollution on the Feeding, Bioturbation and

21

pellets and non- processed soils for chlorophyll a analysis and some for bioturbation

assessment (ii) crab samples were also counted visually and then samples collected for

biomass measurements.

Sediments were collected in 10 ml vials. The vials were covered with an aluminium foil to

prevent further photosynthetic activities. Bioturbated soils were taken to the Kenya Marine

and Fisheries Research Institute (KMFRI) Gazi Station for weighing while the remaining

samples were transported to KMFRI main laboratories in Mombasa for chlorophyll a

analysis. Details on the procedures which took place after the samples were collected are

explained below.

Figure 7: Photo showing quadrats set in the A marina and Desert zones (Photos by Marco)

Page 32: Impacts of Pollution on the Feeding, Bioturbation and

22

Figure 8: Sampling design indicating the sampling zones and transects

3.4.1. Chlorophyll a analysis

Standard methods of measuring Chl a levels in the sediment (Parsons et al., 1984) were used.

One gram of the sediment was taken from each sample of feeding pellets and non-processed

soil. One gram of sediment was then placed in a 15 ml conical tube and 10 ml acetone was

added. The conical tubes were left to stand for 24 hours at 20o C in the dark for extraction of

Chlorophyll a. To facilitate extraction, each tube was put in a centrifuge and mixed at 200 rfc

for 10 minutes immediately after the addition of acetone and after 12 to 15 hours.

Fluorescence of acetone extractions of samples was measured with a Turner Designs

fluorometer, and Chl a content was calculated. Following acetone extraction the sediment

was transferred to pre-weighed aluminium pans, dried at 100oC overnight and weighed. Chl a

Page 33: Impacts of Pollution on the Feeding, Bioturbation and

23

content was calculated per g of sediment. For statistical analysis, the values for the three

cores from each replicate were pooled to obtain one value per replicate.

Fluorescence of the extracts was taken at different wavelengths (630, 647, 664 and 750 nm),

using spectrophotometer from their chlorophyll a content was calculated using the formula

below. The absorbance values at 750 nm was subtracted from the absorbance values at each

of the other three wavelengths (630, 647 and 664 nm) and substituted in the following

equation, this is for purposes of correcting any errors incurred during Spectrophotometer

readings.

Formulae:

[Chl.a]extract 11.85A664/ I 1.54A647

/ I 0.08A630

/ I

Where Chl. a= chlorophyll a, A= corrected absorbance and I= path length in cm.

3.4.2 Bioturbation

Sediment was sampled each replicate transect by collecting five cores 3.5 cm in diameter and

20 cm in depth. Standard weights (100 g) of the different samples were dried at 105oC in the

laboratory. Sediment particles were separated according to grain size using a series of sieves

of 2 mm to 63 mm mesh size mounted on a mechanical shaker and graded according to the

Wentworth scale. The content of each sieve was weighed. Samples collected for analysis of

organic content were ignited at 550oC for 3 h and cooled in desiccators. The loss on ignition

(LOI) was measured and the organic content expressed as a percentage of the dry weight

(Heir et al., 2001). Sediments were collected from the upper few millimeters of the sediment

Page 34: Impacts of Pollution on the Feeding, Bioturbation and

24

since this is where the feeding and other activities like burrowing of the fiddler crabs is

confined (Dye & Lasiak, 1987).

3.4.3 Crab biomass estimation

To estimate crab biomass at the different sampling sites, we collected a total of 117 Uca

annulipes were collected. Carapace width (CW) and length (CL) were determined using

vernier callipers. Samples were then dried in the oven at 100 oC and the dry weight obtained

using a precision balance and their respective sex recorded. The total biomass of each

specimen was estimated by multiplying the average DW and the total number of species

collected. However, it was very difficult for us during this study to estimate the crabs weight

since after they were dried, the crabs reduced their weight.

3.5. Data Analysis

Cochran‟s multiple comparison test of homogeneity was performed on all the data collected.

Data sets collected from the feeding, bioturbation and biomass samples were then tested for

normality using Shapiro‟s test and data transformed [Sqrt (X+1)]. A four factor Analysis of

Variance (ANOVA) was used to determine whether there were differences in feeding,

bioturbation and biomass of the fiddler crab Uca annulipes within the two sites Mikindani

and Gazi. In this study, the following factors were put into consideration when using the

ANOVA tests, Impact vs Control (I vs C, asymmetrical, fixed and orthogonal), site (random

and nested in „I vs C), and transect (random and nested in site) and time which played a very

important role in the data analysis process since we data collection was always dependent on

spring tide season and time. Data was entered into the spread sheet and the graphs were

generated. The statistical package MINITAB 10 was used to calculate the different means.

Page 35: Impacts of Pollution on the Feeding, Bioturbation and

25

CHAPTER 4: RESULTS

4.1 Impacts of urban wastewater on the feeding rate of U. annulipes

In this study it was hypothesised that there is a difference in chlorophyll concentration

between the two locations studied. Results (Fig. 9) show that there is a difference but in terms

of localities and zones. This means that Chl a concentrations are higher in Mikindani than in

Gazi. More Chl a concentrations is found in the Avicennia zone than in the desert of

Mikindani. (F1,88=0.146; p < 0.05). Moreover, there is no significant difference in the Chl a

found in the processed (0.36 ± 0.07) and non- processed soils (0.32 ± 0.07) Avicennia zone.

In the desert zone too minimal variations in Chl a concentration are recorded in non-

processed soil (0.16 ± 0.01) compared to the feeding pellets (0.13 ± 0.01).

Figure 9: Mean ( x ± SE) Chlorophyll a concentration in the processed and non-processed sediments (soil) in

Gazi and Mikindani within the Avicennia marina and desert zones

0

0.05

0.1

0.15

0.2

0.25

0.3

0.35

0.4

0.45

Avicennia Desert Avicennia Desert

mg

Ch

l/

g o

f so

il

pellets

soil

Gazi Mikindani

Page 36: Impacts of Pollution on the Feeding, Bioturbation and

26

4.2 Impacts of urban waste on the bioturbation activity of U. annulipes in human

impacted Mikindani and non-urban Gazi Bay.

Is there a difference in bioturbated material between the impacted (Mikindani) and non

impacted (Gazi)? Four ways ANOVA found differences in bioturbation between the

impacted site (Mikindani) and the control (Gazi). There was a lot more bioturbated materials

in Gazi (F1, 16=70.65; p < 0.05) (Table 1). Generally, higher amounts of feeding material

were removed in Avicennia zone of Gazi (162 ± 90) than in all other zones (Fig. 10). Higher

rate of bioturbation was recorded in Avicennia zone of Gazi than the desert zone (90 ± 60)

while in Mikindani, a higher rate of bioturbated material was recorded in Avicennia zone (36

± 18) in comparison to the desert zone (30 ± 42) (Fig. 10).

0

30

60

90

120

150

180

210

240

270

Avicennia Desert Avicennia Desert

DW

(g

) fe

ed

ing

pe

lle

ts

0

30

60

90

120

150

180

210

240

270

Avicennia Desert Avicennia Desert

DW

(g

) fe

ed

ing

pe

lle

ts

Gazi Mikindani

Figure 10: Mean ( x ± SE) dry weights (g) of feeding pellets collected in Mikindani and Gazi within

the Avicennia marina and desert zone

Page 37: Impacts of Pollution on the Feeding, Bioturbation and

27

Table 1: Results of the four factor-ANOVA conducted on square rooted transformed dry weight (g) of feeding

pellets (used to find bioturbation data) recorded from Mikindani and Gazi.

Source DF MS F P

data 1 28.8854 1.51 0.3438

Impact (I) vs Control

(C) 1 233.7663 70.65

0.0139*

zone (Desert Vs

Avicennia) 1 35.9318 5.86

0.1365

Transects 2 6.1311 0.81

(I vs C)×zone 1 6.9779 2.11

Transect×(I vs C) 2 3.3089 0.44

Data×(I vs C) 1 6.7724 0.58

Data×zone 1 0.1614 0.01

Data ×transect 2 19.0958 2.52

Data×(I vs C)×zone 1 12.3091 1.06

Data×(I vs

C)×transect 2 11.619 1.53

Result 16 7.5927

Total 31

*p< 0.05

4.3 Impact of pollution on Uca annulipes biomass

The four-way ANOVA tests on Uca annulipes total crab biomass are presented (Table 2). Is

there any difference in Uca annulipes biomass between human impacted Mikindani and Gazi

which is a non urban site? This was a no and yes situation. The total crab biomass was higher

in the Avicennia than in the desert zone in both sites (F1,16=75.28, p>0.05) (Fig. 11), with

higher total biomass being recorded in the Avicennia of Mikindani than in any other zone of

the two sites (F1,16=54.48, p<0.05) (Table 2). Further analysis was carried out to find out if

there was any relation in bioturbated material (both expressed as the feeding pellets and

Page 38: Impacts of Pollution on the Feeding, Bioturbation and

28

excavated materials- non processed soils), and the crab biomass in the two sites (Fig. 12).

However, there was no relationship between the mass of bioturbated material and Uca

biomass (R2

=0.0197, p < 0.05). Results also show that the amount of excavated material did

not relate to the Uca biomass (R2 = 0.0248, p < 0.05) (Fig. 12).

Figure 11: Mean ( x ± SE) dry weights (g) of Uca annulipes (biomass) collected in Mikindani and

Gazi within the Avicennia marina and desert zone

Gazi Mikindani

0

1

2

3

4

5

6

7

8

9

10

Avicennia Desert Avicennia Desert

DW

(g

) U

ca

0

1

2

3

4

5

6

7

8

9

10

Avicennia Desert Avicennia Desert

DW

(g

) U

ca

Page 39: Impacts of Pollution on the Feeding, Bioturbation and

29

Table 2 : Results of the four factor-ANOVA conducted on square rooted transformed biomass (Expressed as

Dry Weight (DW) data from Mikindani and Gazi

DF Dry Weight (DW

Source MS F

Time 1 0.52 6.7

Impact (I) vs Control (C) 1 0.8079 18.95

zone (Desert Vs Avicennia) 1 8.2322 75.28*

Transects 2 0.1094 1.72

(I vs C)×zone 1 2.3225 54.48*

Transect×(I vs C) 2 0.0426 0.67

Time×(I vs C) 1 0.2231 1.24

Time×zone 1 0.8079 10.41

Time ×transect 2 0.0776 1.22

(I vs C)×zone×Time 1 0.0868 0.48

Time×(I vs C)×transect 2 0.1793 2.82

Result 16 0.0636

Total 31

*p< 0.05

Page 40: Impacts of Pollution on the Feeding, Bioturbation and

30

Figure 12: The dry weight of bioturbated material in relation to Fiddler crab U. annulipes biomass

y = -3.9224x + 86.824

R2 = 0.0197

0

50

100

150

200

250

300

350

0 2 4 6 8 10 12

DW (g) Uca

DW

(g)

feedin

gp

ellets

y = -0.6129x + 13.07

R2 = 0.0248

0

5

10

15

20

25

30

0 2 4 6 8 10 12

DW (g) Uca

DW

(g)e

xcasvate

dm

ate

ria

l

y = -3.9224x + 86.824

R2 = 0.0197

0

50

100

150

200

250

300

350

0 2 4 6 8 10 12

DW (g) Uca

DW

(g)

feedin

gp

ellets

y = -3.9224x + 86.824

R2 = 0.0197

0

50

100

150

200

250

300

350

0 2 4 6 8 10 12

DW (g) Uca

DW

(g)

feedin

gp

ellets

y = -0.6129x + 13.07

R2 = 0.0248

0

5

10

15

20

25

30

0 2 4 6 8 10 12

DW (g) Uca

DW

(g)e

xcasvate

dm

ate

ria

l

y = -0.6129x + 13.07

R2 = 0.0248

0

5

10

15

20

25

30

0 2 4 6 8 10 12

DW (g) Uca

DW

(g)e

xcasvate

dm

ate

ria

l

Page 41: Impacts of Pollution on the Feeding, Bioturbation and

31

CHAPTER 5: DISCUSSION

In the Kenya, the coastal town of Mombasa is reported to face serious challenges of sewage

pollution. Mombasa city has only one sewage treatment facility which had previously stalled

for several years and is currently working at 50 % capacity after renovation (Okuku et al.,

2011). This 50 % capacity can barely serve even 12 % of the Mombasa city population

leading to volumes of sewage being discharged either untreated or slightly treated (Okuku et

al., 2011). In this study two major points were emphasised in discussing the results, first is

that the use of stratified sampling design adapted to the natural zonation of East Africa

mangrove forests (Kathiresan and Bingham, 2001; Dahdough-Guebas et al., 2002), allowed

us to compare relatively homogenous area in terms of vegetation cover and flooding regime,

and the second is that there is high variation in Uca crab assemblage both at spatial and

temporal scales, and Kenya has a higher ocypodid biomass.

Crabs can process the surface of the most if not all of the intertidal zone in one tidal cycle

(personal observation). It is clear from this study that crabs feeding at observed field densities

can significantly reduce Chl a levels. Generally there the effect of crab feeding was

pronounced in Gazi than in Mikindani. However, Chl a concentration remained constant in

Gazi both in Avicennia and Desert zones, an in the feeding pellets and non processed soil. In

Mikindani feeding was pronounced in the Desert zone, than in the Avicennia zone. It is

interesting to note that high concentrations of Chl a was measured in the feeding pellets of

the Avicennia zone of Mikindani. Fiddler crabs are known to consume benthic microalgae,

therefore they reduce the Chl a content in the sediment (Reinsel, 2004). Studies carried by

Reinsel (2004) in Rachel Estuary, North Carolina, where Uca pugilator foraging on sand flats

reduced sediment Chl a by 20 %. Robertson et al. (1980), also reported 70 % reductions of

Page 42: Impacts of Pollution on the Feeding, Bioturbation and

32

Chl a by Uca pugilator in Georgia sand flats. My studies are similar to those of Reinsel

whose sediment samples were mixtures of feeding pellets and non processed soils. Thus the

values of this study represent a combination of the crabs‟ ability to remove food from the

sediment and processed sediments.

Kenya has been reported to have higher Uca crab biomass (Cannicci et al., 2009). This study

accounted for random variability between the non urban and peri urban sites. Indeed, the high

concentrations of anthropogenic nutrients and pollutants introduced in the system of

Mikindani in urban sewage did not appear to stress the crabs. The nutrient concentration in

the two study sites has been reported in studies by Okuku et al. (2011). Nutrient

concentrations were found to be higher in Tudor creek (means of 0.163 mg/L Nitrate +

Nitrites and 0.11 mg/L ammonium), compared to Gazi‟s (means of 0.019 mg/L Nitrate +

Nitrites and 0.018 mg/L ammonium). At Mikindani different Uca biomass relative to control

sites were only found in the Avicennia zone and the Desert Zone. These results are consistent

with the observation that dumping of sewage at Mikindani affects primarily the landward

Avicennia belt which is the desert zone (Mohamed et al., 2008). The soils and vegetation of

the desert zone which is more landward can efficiently assimilate the overload of nutrients

(Tam and Wong, 1995; Wong et al., 1997). The desert zone at Mikindani may be acting as a

phytoremediation system, which is mitigating the effect of the wastewater.

It is also important to state that in both Gazi and Mikindani, the crab biomass was higher in

the Avicennia zone than the Desert zone, this confirms that Uca annulipes are inhabitants of

the Avicennia marina zone as earlier indicated in this study. However, high biomass of fiddler

crab at the peri-urban site may be directly linked to the enhanced nutrients concentrations

from sewage loading. The nutrients increase benthic diatoms and bacteria upon which the

Page 43: Impacts of Pollution on the Feeding, Bioturbation and

33

Uca annulipes feed (Meziane and Tsuchiya, 2002). Data from this study not only confirms

the dominance of Uca annulipes in Kenya, found by Hartnoll et al. (2002).

In this study it was found out that crab biomass was not affected by the pollution stress.

Therefore we saw it necessary to find out if the amount of feeding pellets and the excavated

material was related to the biomass. Results showed that there was no relationship between

the mass of bioturbated material and the Uca biomass. In addition, we did not find any

relationship between the excavated material and the Uca biomass. Previous studies by

Reinsel (2004) using Uca pugilator found that fiddler crab activity takes place in small areas

where they feed and also in the sediment they do not process during given tidal cycle

making it difficult to measure the effects of their activity.

Tidal effect also play a major role in the renewal of crab activity in one tidal cycle, therefore

there is no enough time between feeding periods for regeneration to occur. When tides

recede the crabs carry out their activities of feeding and excavation of the burrows.

However, where high tides come, it washes away all the sediment (Reinsel, 2004).

Page 44: Impacts of Pollution on the Feeding, Bioturbation and

34

CHAPTER 6: CONCLUSIONS AND RECOMMENDATIONS

6.1 CONCLUSIONS

The present results show that the mangrove crabs are affected by pollution this is contrast

to findings of Yu et al. (1997) in Futian mangroves. Notable patterns were observed at the

peri- urban site compared to the control, where there was a consistent increase in Chl a

concentration at the peri-urban site. On the other had crab biomass was higher both in

Avicennia zone of the impacted site and the control. Moreover, from ecological point of

view it can be concluded that the steady increase in crab biomass which was observed at

the peri-urban site (Mikindani) did not indicate that the system was healthier. This kind of

alteration in biomass can lead to unsustainable alterations in ecosystem function (Duke et

al., 2007). Therefore, data from this study are important for management of peri-urban

mangrove areas, since fiddler crabs play a significant role in the control of algal mat

growth in mangrove substrata. Fiddler crabs through feeding, burrowing and ventilation

activities have an influence on microbial activity and sediment metabolism in marine

sediments (Aller and Aller, 1998).

Page 45: Impacts of Pollution on the Feeding, Bioturbation and

35

6.2 RECOMMENDATIONS

Sewage pollution is considered one of the greatest threats to coastal and marine ecosystems in

the East African region. Therefore, there is need to study tropical mangals not only from the

perspective of impact of physical or biotic forces alone. Studies carried in the mangals should

be integrative focusing on ecotoxicological information on the impact of chemical

contaminants on biodiversity. This will provide basis for serious environmental impact

assessments in cases of project implementations like ports and harbours, rice farms.

Different weight of evidence approach can also be applied where by the different organisms

are studies through different lines of evidence namely toxicity in the laboratory, in situ and

bioaccumulation and biomagnifications. The ecotoxicological information will also be

important for future pollution management policies.

Page 46: Impacts of Pollution on the Feeding, Bioturbation and

36

REFERENCES

Abuodha, P. and Kairo, J.G. 2001. Human-induced stresses on mangrove swamps along

Kenyan coast. Hydrobiologia, 458: 255-265.

Adeel, Z. and Pomeroy, R. 2002. Assessment and management of mangrove ecosystems in

developing countries. Trees, 16: 235-238.

Aller, R. C. and Aller, J. Y. 1998. The effect of biogenic irrigation intensity and solute

exchange on diagenetic reaction rates in marine sediments. Journal of Marine

Research, 56: 905-936.

Ashton, E. C., Macintosh, D. and Hogarth, P. J. 2003. A baseline study of the diversity and

community ecology of crab and molluscan in the Sematan mangrove forest, Sarawak,

Malaysia. Journal of Tropical Ecology, 19: 1-16.

Bergey, L.L and Weiss, J.S. 2008. Aspects of population ecology in two populations of

fiddler crabs, Uca pugnax. Marine Biology, 154: 435-442.

Bilyard, GR 1987. The value of benthic infauna in marine pollution monitoring studies.

Marine Pollution Bulletin, 18: 581–585.

Bosire, J.O., Dahdouh, F., Kairo, J. G., Cannicci, S., and Koedam, N. 2004. Spartial

variations in macrobenthic fauna recolonization in a tropical mangrove bay.

Biodiversity and Conservation, 13:1059-1074.

Botto, F., Iribarne, O. 2000. Contrasting effect of two burrowing carbs (Chasmagnathus

granulata and Uca uruguayensis) on sediment composition and transport in estuarine

environments. Estuarine Coastal and Shelf Science, 51: 141–151.

Cannicci, S., Fabrizio, B., Dahdouh-Guebas, F., Fratini, S.,Litulo, C., Macia, A., Mrabu, E.J.,

Lopes, P. G., Paula, J. 2009. Effects of Urban wastewater on crab and mollusc

assemblages in equitorial and subtropical mangroves of East Africa. Estuarine

Coastal and Shelf Science, 21: 1-13.

Cannicci,S., Burrows D., Fratini, S., Lee, S.Y., Smith, T.J III., Offenberg, J., Dahdouh-

Guebas, F. 2008. Faunistic impact on vegetation structure and ecosystem function in

mangroves forests: a review. Aquatic Botany, 89: 186-200.

Chapman, M.G and Tolhurst, T.J. 2004. The relationship between invertebrate assemblages

and bio-dependent properties of sediment in urbanized temperate mangrove forests.

Journal of Experimental Marine Biology and Ecology, 304: 51-73.

Chapman,V.J. 1944.The 1939 Cambridge university expedition to Jamaica. Journal of

Linnean Society, Botany, LII 346: 407-533

Clark, R.B., Frid, C. and Attrill, M. 2001. Marine pollution, 5th

Edition 1-145. Oxford

University press. Oxford

Page 47: Impacts of Pollution on the Feeding, Bioturbation and

37

Clough, B.F., Boto, K.G. and Attiwell, P.M. 1983. Mangroves and sewage: a reevaluation.In:

Teas, H. (Ed.), Tasks for Vegetation Science, vol. 8. Dr. W. Junk Publishers, The

Hague, pp. 151–161.

Culbertson, J. B.,Valiela, I., Emily E. P., Christopher M. R., Anna., C. and Rachel V.K. 2007.

Long-term biological effects of petroleum residues on fiddler crabs in salt marshes.

Marine Pollution Bulletin, 54: 955–962.

Dahdouh-Guebas, F., Giuggioli, M., Oluoch, A., Vannini, M. and Cannicci, S. 1999. Feeding

habits of non-ocypodid crabs from two mangrove forests in Kenya. Bulletin of Marine

Science, 64: 291-297.

Dahdouh-Guebas, F., Verneit, M., Cannicci, S., Kairo, J. G., Track, J. F. and Koedam, N.

2001. An explatory study on grapsid crab zonation in mangrove forests in Kenya.

Wetlands Ecology and Management, 10: 179-187.

Dahdouh-Guebas, F.,Jayatissa, L.P., Di Nitto, D., Bosire, J.O., Seen, D.L., Koedam,N.2005.

How effective were mangroves as defence against the recent tsunami? Current

Biology, 15: 443-447.

De Wolf, H., Ulomi, S.A., Pratab, H.B and Blust, R. 2000. Heavy Metal levels in the

sediments of four Dar es Salaam mangroves.Accumulation in and effect on the

morphology of the periwinkle Littoraria scabra (Mollusca:Gastropoda). Environment

International, 26: 243-249.

Dittmann, S. 1996. Effects of macrobenthic burrows on in faunal communities in tropical

tidal flats. Marine Ecology Progress Series, 134: 119–130.

Duke, N.C., Meynecke, J.O., Dittmann, S., Ellison, A.M., Anger, K., Berger, U., Cannicci,

S., Diele, K., Ewel, K.C., Field, C.D., Koedam, N., Lee, S.Y., Marchand, C.,

Nordhaus, I. and Dahdouh-Guebas, F. 2007. A world without mangroves? Science,

317: 41–42.

Duke, N.C.1992. Mangrove floristics and biogeography. Pp 63-100 n: Robertson AI, Alongi

DM (eds.) Tropical mangrove ecosystems. American Geophysical Union, Washington

DC, USA

Dye, A. H., Lasiak, T. A. 1987. Assimilation efficiencies of fiddler crabs and deposit-feeding

gastropods from tropical mangrove sediments. Comparative Biochemistry and

Physiology, 87: 341-344.

FAO.2005 Global forest resource assessment: progress towards sustainable forest

management. FAO Forestry Paper 147, Rome, pp 348.

Farnsworth, E.J. and Ellison, A.M. 1996. Scale-dependent spatial and temporal variability in

biogeography of mangrove root epibiont communities. Ecological Monographs, 66:

45–66.

Fondo, E and Martens, E 1998. Effects of Mangrove deforestation on macrofaunal densities

in Gazi Bay, Kenya. Mangroves and Salt Marshes, 2: 75-81.

Page 48: Impacts of Pollution on the Feeding, Bioturbation and

38

Fratini, S., Vannini, M., Cannicci, S. and Schubart, C.D. 2005. Tree-climbingmangrove

crabs: a case of convergent evolution. Evolutionary Ecology Research, 7: 219–233.

Fratini, S., Vigiani, V., Vannini, M. and Cannicci, S. 2004. Terebralia palustris (Gastropoda;

Potamididae) in a Kenyan mangal: size structure, distribution and impact on the

consumption of leaf litter. Marine Biology, 144: 1173–1182.

Garmouma, M., Teil, M.J., Blanchard, M., Chevreuil, M. 1998. Spatial and temporal

variations of herbicide (triazines and phenylureas) concentrations in the catchment

basin of the Marine river (France). Science of the Total Environment, 224: 93-107.

GESAMP. 1990. State of the marine environment, report and studies, No.39, (p.111).

Nairobi: UNEP.

Glaser, M. 2003. Interrelations between mangrove ecosystems, local economy ad social

sustainability in Caete´ Estuary, North Brazil. Wetlands. Ecology and Management,

11: 265–272.

GOK. 2005. MOMBASA District Strategic Plan 2005–2010 for implementation of the

national population policy for sustainable development. National Coordinating

Agency for Population and Development, p 57.

Gutiérrez, J.L., Jones, C.G.,Groffman,P.M.,Findlay, S.E.G., Iribarne,O.O.,Ribeiro, P.D.,

Bruschetti,C.M. 2006. The contribution of crab burrow excavation to carbon

availability in surficial salt-marsh sediments. Ecosystems, 9: 647-658.

Hartnoll, R.G., Cannicci, W. D., Emmerson., Fratini, S., Macia, A., Mgaya, F., Ruwa, R.K.,

Shunnula, J. P., Skov, M. W and Vannini, M. 2002. Geographic trends in mangrove

crab abundance in East Africa. Wetlands Ecology and Management, 10: 203-213.

Hartnoll, R.G.1988.Eco-ethology of mangroves. Pp 477-489 in: Chelazzi G, Vannini M (eds.)

Behavioural adaptations to intertidal life. NATO ASI Series A, vol 151. Plenum Press,

New York.

Heiri, O., Lotter, A.F and Lemcke, G. 2001. Loss on ignition as a method for estimating

organic and carbonate content in sediments: reproducibility and comparability of

results. Journal of Paleolimnology, 25: 101-110.

Hogarth ,P.J.1999.The biology of mangroves. Oxford University press, New York. Pp 228

Hogarth, P.J. 2007. The Biology of Mangroves and Seagrasses. Oxford University Press,

New York.

Howes, B.L. and Goehringer, D.D. 1994. Porewater drainage and dissolved organic carbon

and nutrient loss through the intertidal creek banks of a New England salt marsh.

Marine Ecology Progress Series, 114: 289–301.

Hunter,C and Evans, C.W. 1995. Coral reefs in Kaneoche Bay, Hawaii: two centuries of

western influence and two decades of data. Bulletin of Marine Science, 57: 501-515.

Page 49: Impacts of Pollution on the Feeding, Bioturbation and

39

Icely, J. D. and Jones, D. A. 1975. Factors affecting the distribution of the genus Uca

(Crustacea: Ocypodidae) on East African Shore. Estuarine Coastal Marine Science, 6:

315-325.

Inglis, G.J and Kross, J.E. 2000. Evidence for Systemic Changes in the Benthic Fauna of

Tropical Estuaries as a Result of Urbanization. Marine Pollution Bulletin, 41(7-12),

367-376.

Jenssen, B.J. 2003. Marine Pollution: the future challenges is to link human and wildlife

studies-Guest Editorial. Environmental Health Perspectives, 111: A198.

Kairo, J. G. 2001. Ecology and restoration of mangrove systems in Kenya. Ph. D. Thesis.

Laboratory of Plant Sciences and Nature Management, University of Brussels (VUB),

Belgium.

Kairo, J.G., Bosire, J., Mohammed, O.S. 2005. Assessment of the effects of oil spill on the

mangrove forests of Port Reitz, Mombasa. Kenya Marine and Fisheries Research

Institute. Mangrove System Information Service, Mombasa.

Kathiresan, K. and Bingham, B.L. 2001. Biology of mangroves and mangroves ecosystems.

Advances in Marine Biology, 40: 84–251.

Kitheka, J. U., Ohowa, B.O., Mwashote, B.M., Shimbira, W. S., Mwaluma, J. M. and

Kazungu, J. M. 1996. Water circulation dynamics, water column nutrients and

plankton productivity in a well-flushed tropical Bay in Kenya. Journal of Sea

Research, 35: 257-268.

Kitheka, J.U. 1996. Water circulation and coastal trapping of brackish water in a tropical

mangrove-dominated bay in Kenya. Limnology and Oceanography, 41: 169-176.

Kitheka, J.U., Ongwenyi, G.S. and Mavuti, K.M. 2003. Fluxes and exchange of suspended

sediment in tidal inlets draining a degraded mangrove forest in Kenya. Estuarine

Coastal and Shelf Science, 56: 655–667.

Kokwaro, J. O. 1985. The distribution and economic importance of mangrove forests of

Kenya. Journal of East Africa Natural History Society and National Museums, 75: 1-

10.

Kristensen, E. 2008. Mangrove crabs as ecosystem engineers; with emphasis on sediment

processes. Journal of Sea Research, 59: 30-43

Kristensen,E., Bouillon, S, Dittmar, T., Marchand, C. 2008. Organic Carbon dynamics in

mangrove ecosystems: a review. Aquatic Botany, 89: 201-219.

Lee, S. Y. 1998. Ecological role of grapsid crabs in mangrove ecosystems: a review Marine

Freshwater Research, 49: 335-343.

Litulo, C. 2005. Population biology of the fiddler crab Uca annulipes

(Brachyura:Ocypodidae) in a tropical East African mangrove (Mozambique).

Estuarine, Coastal and Shelf Science, 62: 283-290.

Page 50: Impacts of Pollution on the Feeding, Bioturbation and

40

Lugo, A.E and Snedaker SC.1974. The ecology of mangroves. Annual Review of Ecology and

Systematics, 5: 39-65

Macia, A. Quincardete, I. and Paula, J. 2001. A comparison of alternative methods for

estimating population density of the fiddler crab Uca annulipes at Sacco mangrove,

Inhaca Island, Mozambique. Hydrobiologia, 449: 213-219.

MacNae, W.1968. A general account of the fauna and flora of mangrove swamps and forests

in the Indo-West-Pacific region. Advances in Marine Biology, 6: 73-270.

McCraith, B.J., Gardner, L.R., Wethey, D.S., Moore, W.S. 2003. The effect of fiddler crab

burrowing on sediment mixing and radionuclide profiles along a topographic gradient

in a southeastern salt marsh. Journal or Marine Research, 61: 359-390.

Meziane, T and Tsuchiya, M. 2002. Organic matter in a subtropical mangrove- estuary

subjected to wastewater discharge: origin and utilisation by two macro-zoobenthic

species. Journal of Sea Research, 47: 1-11.

Micheli, F., Gherardi, F and Vannini, M. 1991. Feeding and barrowing ecology of two East

African mangrove crabs. Marine Biology, 3: 247-254.

Mohamed, M.O.S. 2008. Are peri-urban mangrove forests viable? Effects of Domestic

Sewage Pollution On The Structure And Development Of The Mangroves of

Mombasa (Kenya). Ph.D. Thesis, Vrije Universiteit Brussel – Universite ´ Libre de

Bruxelles, Belgium, 183 pp.

Mohamed, M.O.S., Neukermans, G., Kairo, J.G., Dahdouh-Guebas, F. and Koedam, N. 2008.

Mangrove forests in a peri-urban setting: the case of Mombasa (Kenya). Wetlands

Ecology and Management. doi:10.1007/s11273-008-9104-8.

Mwaguni, S. and Munga, D. 1997. Land based sources and activities affecting the quality and

uses of the Marine coastal and associated freshwater environments along the Kenya

coast. Coastal Development Authority.

Nagelkerken, I., Blaber, S., Bouillon, S., Green, P., Haywood, M., Kirton, L.G., Meynecke,

J.O., Pawlik, J., Penrose, H.M., Sasekumar, A. and Somerfield, P.J. 2008. The habitat

function of mangroves for terrestrial and marina fauna: a review. Aquatic Botany, 89:

155–185.

Nielsen, O.I., Kristensen, E., Macintosh, D.J. 2003. Impact of fiddler crabs (Uca spp.) on

rates and pathways of benthic mineralization in deposited mangrove shrimp pond

waste. Journal of Experimental Marine Biology and Ecology, 289: 59–81.

Nobbs, M and McGuinness, A. 1999. Developing methods for quantifying the apparent

abundance of fiddler crabs (Ocypodidae: Uca) in mangrove habitats. Australian

Journal of Ecology, 24: 43-49.

Odum, W.E, McIvor, C.C, Smith TJ. 1985. The ecology of mangroves of South Florida: a

community profile. US Fish and Wildlife Service, Office of Biology series.

Washington DC. FWS/OBS-81/24

Page 51: Impacts of Pollution on the Feeding, Bioturbation and

41

Okuku, E.O., Ohowa, B., Mwangi, S.N., Munga D., Kiteresi, L.I., Wanjeri, V.O., Okumu, S

and Kilonzi, J. 2011. Sewage pollution in the Coastal waters of Mombasa City,

Kenya: A norm rather than an exception. International Journal of environment

Research. 5 (4): 865-874, Autumn 2011.

Olafsson, E. and S. G.M. Ndaro. 997. Impact of mangrove crabs Uca annulipes and Dotilla

fenestra on meiobenthos. Marine Ecology Progress Series, 158: 225-231.

Palanisamy, S., Neelamani, S., Yu-Hwan, A., Ligy, P and Gi-Hoon, H. 2007. Assessment of

the levels of coastal marine pollution of Chennai City, Southern India. Water

Resources Management, 21: 1187-1206.

Parson, T. R., Maita, Y. and Lalli, C. M. 1984. A Manual of chemical and biological methods

for seawater analysis. Pergamon.

Por, F.D, Dor, I (eds.).1984. Hydrobiology of the mangal. Dr W Junk Publishers, The Hague.

ISBN 90 6193 771 X. 251 p

PUMPSEA. 2007. Peri-urban mangrove forests as filters and potential phytoremediators of

domestic sewage in East Africa. Project number: INCO-CT2004- 510863, Second

Periodic Activity Report, 28 pp.

Reinsel, K. A. 2004. Impact of fiddler crab foraging and tidal inundation on an intertidal sand

flat: Season-dependent effects in one tidal cycle. Journal of Experimental Marine

Biology and Ecology, 313: 1-17.

Ridd, P.V.1996. Flow trough animal burrows in mangrove creeks. Estuarine Coastal Shelf

Science, 43: 617–625.

Rivera–Monroy, V.H. and Twilley, R.R. 1996. The relative role of denitrification and

immobilization in the fate of inorganic nitrogen in mangrove sediments (Terminos

Lagoon, Mexico). Limnology and Oceanography, 41: 284–296.

Robertson, J.R., Bancroft, K., Vermeer, G. and Plaisier, K. 1980. Experimental studies on the

foraging behavior of the sand fiddler crab Uca pugilator (Bosc, 1802). Journal of

Experimental Marine Biology and Ecology, 44: 67– 83.

Robertson, J.R., Bancroft, K., Vermeer, G., Plaisier, K. 1980. Experimental studies on the

foraging behaviour of the sand fiddler crab Uca pugilator (Bosc, 1802). Journal of

Experimental Marine Biology and Ecology, 44: 67-83.

Ruwa, R. K. 1997. Zonation of burrowing crabs in the mangroves of the east coast of Kenya.

In: Kjerve, Bjorn, Luiz Drude de Lacerda and El Hadji Salif Diop, (eds.), Mangrove

ecosystem studies in Latin America and Africa. Unesco Technical paper in Marine

Science.

Scholander, P.F, van Dam L, Scholander, S.I.1955.Gas exchange in the roots of mangroves.

American Journal of Botany, 42: 92-98

Seitzinger, S.P., Harrison, J.A., Dumont, E., Beusen, A.H.W and Bouman, A.F. 2005. Source

and delivery of carbon, nitrogen and phosphorus to the coastal zone: an overview of

Page 52: Impacts of Pollution on the Feeding, Bioturbation and

42

Global Nutrient Export from Watersheds (NEWS) models and their application.

Global Biogeochemistry Cycles, 19: 1-2.

Sheridan, P. and Hays, C. 2003. Are mangroves nursery habitat for transient fishes and

decapods? Wetlands Ecology and Management, 23: 449–458.

Shunula, J. P .2002. Public awareness, key to mangrove management and conservations: the

case of Zanzibar.

Shunula, J.P and Whittick, A. 1999. Aspects of litter production in mangroves from Unguja

Island, Zanzibar, Tanzania. Estuarine Coastal Shelf Science, 49 (supplement): 51-54

Skov, M. W. and Hartnoll, R. 2002. Paradoxical selective feeding on a low-nutrient diet: why

do mangrove crabs eat leaves? Oecologia, 131: 1-7.

Skov, M.W., Vannini, M., Shunula, J.P., Hartnoll, R.G. and Cannicci, S. 2002. Quantifying

the density of mangrove crabs: Ocypodidae and Grapsidae. Marine Biology, 141: 725

- 732.

Stieglitz, T., Ridd, P. and Müller, P. 2000. Passive irrigation and functional morphology of

crustacean burrows in a tropical mangrove swamp. Hydrobiologia, 421: 69 - 76.

Subramanian, B.R.1999. Status of marine pollution of India. In Proceeding of Indo-British

integrated coastal zone management training short-course conducted by Institute for

Ocean Management, Anna University.

Tam NFY, Wong YS 1999 Mangrove soils in removing pollutants from municipal

wastewater of different salinities. Journal of Environmental Quality, 28: 556 - 564

Tam, N. F. Y. and Wong, Y. S. 1996. Retention of wastewater-borne nitrogen and

phosphorus in mangrove soils. Environmental Technology, 17: 851-859.

Tomlinson, P.B. 1986.The botany of mangroves. Cambridge Tropical Biology Series,

Cambridge University Press, Cambridge. Pp 419.

Trott, L.A., McKinnon, A.D., Alongi, D.M., Davidson, A. and Burford, M.A. 2004. Carbon

and nitrogen processes in a mangrove creek receiving shrimp farm effluent.

Estuarine, Coastal and Shelf Science, 59: 197–207.

Underwood, A.J. 1992. Beyond BACI: the detection of environmental impact on populations

in the real, but variable, world. Journal of Experimental Marine Biology and Ecology,

161: 145-178.

Underwood, A.J. 1994. On beyond BACI: sampling design that might reliably detect

environmental disturbances. Ecological Applications, 4: 3-15.

UNEP .1998. Eastern Africa atlas of coastal resources. Kenya. UNEP, Nairobi Kenya.

UNEP. 2006. The state of the marine environment-trends and processes. United Nations

Environment Programme and the Global Programme of Action for the Protection of

the Marine Environment from Land-based Activities (GPA) of the United Nations

Environment Programme (UNEP), The Hague. 52 p.

Page 53: Impacts of Pollution on the Feeding, Bioturbation and

43

UNEP/GPA., 2000. Cost benefit analysis case studies in Eastern Africa, for the Strategic

action plan on Sewage. UNEP, Eastern Afrian Action Plan/Regional coordinating

unit, The Hague.

Valiela, I., Bowen, J. L. and York, J.K. 2001. Mangrove forests: one of the worlds threatened

major tropical environments. Bioscience, 51: 807-815.

Vijay, R., Sardar. V.K., Dhage, S.S., Kelkar, P.S and Gupta, A. 2010. Hydrodynamic

assessment of sewage impact on water quality of Malad Creek, Mumbai, India.

Environment Monitoring Assessment, 165: 559-571.

Walters, B.B., Ro¨nnba¨ck, P., Kovacs, J., Crona, B., Hussain, S., Badola, R., Primavera, J.,

Barbier, E.B. and Dahdouh-Guebas, F. 2008. Ethnobiology, socioeconomics and

adaptive management of mangroves: a review. Aquatic Botany, 89: 220–236.

Warren, J.H. 1990. Role of burrows as refuge from subtidal predators of temperate mangrove

crabs. Marine Ecology Progress Series, 67: 295-299.

Wolanski E, Spagnol S, Thomas S, Moore K, Alongi D.M, Trott L, Davidson A. 2000.

Modelling an dvisualising the fate of shrimp pond effluent in a mangrove-fringed tidal

creek. Estuarine Coastal Shelf Science, 50: 85-97.

Wolanski, E., Mazda, Y. and Ridd, P. 1992. Mangrove hydrodynamics. In: Robertson, A.I.,

Alongi, D.M. (Eds.), Tropical Mangrove Ecosystems. American Geophysical Union,

Washington, DC, pp. 43–62.

Wolfrath, B. 1992. Field experiments on feeding of European fiddler crab Uca tangeri.

Marine Ecology Progress Series, 90: 39–43.

Wong, Y.S., Lan, C.Y., Che, S.H., Li, X.R., Tam, N.F.Y. 1995. Effects of wastewater

discharge on nutrient contamination of mangroves soil and plants. Hydrobiologia,

295: 243-254.

Wong, Y.S., Tam, N.F.Y. and Lan, C.Y. 1997. Mangrove wetlands as wastewater treatment

facility: a field trial. Hydrobiologia, 352: 49–59.

Yang, Q., Tam, N.F.Y., Wong, Y.S., Luan, T.G., Su, W.S., Lan, C.Y., Shin, P.K.S., Cheung,

S.G., 2008. Potential use of mangroves as constructed wetland for municipal sewage

treatment in Futian, Shenzhen, China. Marine Pollution Bulletin, 57: 735-743.

Yu, R.Q., Chen, G.Z., Wong, Y.S., Tam, N.F.Y., Lan, C.Y. 1997. Benthic macrofauna of the

mangrove swamp treated with municipal wastewater. Hydrobiologia, 347: 127-137.