1

THE ROLE OF NURSERY HABITATS IN THE

EFFECTIVENESS OF MARINE PROTECTED

AREAS IN THE PHILIPPINES

Dirkje Verhoeven

August 2016

2

THE ROLE OF NURSERY HABITATS IN THE

EFFECTIVENESS OF MARINE PROTECTED

AREAS IN THE PHILIPPINES

Dirkje Verhoeven

August 2016

Aquaculture and Fisheries

Supervisors:

ir. A. Andringa-Davis (MCP)

ir. D. Andringa (MCP)

Advisor:

dr. ir. L.A.J. Nagelkerke

The MSc report may not be copied in whole or in parts without the written permission of the author

and the chair group.

ii

ACKNOWLEDGEMENTS

I would like to thank my supervisors of Marine Conservation Philippines (Annelies Andringa and Dolf

Andringa) and Wageningen University (Leo Nagelkerke) for their guidance during this project, Jorien

van Schie, Emily Cook, Kallum Wright, Melina Lemonakis, Rosaly van Dansik, Jessica Odell, Jelle Rienstra

and Anna Pfofenhauer for their support in the field, and Soren Knudsen and Helle Larsen for their

logistical support. Furthermore, I would also like to thank Foundation for Research on Nature

Conservation (FONA) and Stichting Thurkowfonds for their financial support.

iii

ABSTRACT

Reef ecosystems are recognized as one of the most vulnerable marine ecosystems on the planet as

they are highly sensitive to environmental changes. Presence of nursery habitats (mangroves and

seagrass beds) is found to positively affect the reef community structure, abundance of fish species

and biomass of fish, even more than protection status of the reserve. However, the role of nursery

habitats in the Philippines is poorly studied. I tested the hypotheses that (1) the diversity of nursery

fish species on coral reefs increases with increasing connectivity between reef and nursery habitat; (2)

the diversity of nursery fish species on coral reefs increases with increasing size of the nursery habitat;

and, (3) the diversity of nursery fish species on coral reefs is higher in MPAs than in non-MPAs.

Abundance of adult nursery fish species was measured using the belt transect method on nine reefs in

southern Negros Oriental, the Philippines. Presence and abundance of nursery fish species was indeed

related to size and connectivity of nursery habitat. The hypotheses that nursery fish species diversity

increases with size and connectivity of mangrove forest and conservation status, were supported by

the results. More than two-fifth of the fish species affected by connectivity and size of mangrove forest

were important reef community species with high fishery value for fishermen. This study indicates the

importance of mangrove forests for nursery fish species and, hence, reef fish communities in the

Philippines. In order to promote reef fish communities and local fishery resources, this study suggests

that protection of mangrove forests and coral reefs is key.

iv

TABLE OF CONTENTS

INTRODUCTION ....................................................................................................................................... 5

METHODS ................................................................................................................................................ 8

STUDY SITE........................................................................................................................................... 8

SAMPLING DESIGN .............................................................................................................................. 8

NURSERY FISH SPECIES .................................................................................................................... 9

FISH MONITORING ........................................................................................................................ 10

MANGROVE AND SEAGRASS HABITAT MAPPING ......................................................................... 10

DATA ANALYSIS ................................................................................................................................. 11

RESULTS ................................................................................................................................................. 12

FISH SPECIES PRESENCE ..................................................................................................................... 12

FISH ABUNDANCE .............................................................................................................................. 14

FISH SPECIES DIVERSITY ..................................................................................................................... 14

DISCUSSION ........................................................................................................................................... 16

FISH SPECIES PRESENCE AND ABUNDANCE ...................................................................................... 16

FISH SPECIES DIVERSITY ..................................................................................................................... 17

STRENGTHS AND LIMITATIONS OF THE STUDY ................................................................................. 17

PRACTICAL IMPLICATIONS FOR MARINE CONSERVATION ................................................................ 18

RECOMMENDATIONS FOR FUTURE RESEARCH ................................................................................. 18

CONCLUSION ..................................................................................................................................... 19

REFERENCES .......................................................................................................................................... 20

APPENDIX I: SELECTED FISH SPECIES ..................................................................................................... 25

5

INTRODUCTION

Biodiversity loss is one of the greatest environmental concerns of recent days, with a current rate of

extinction occurring at 100 times the natural rate, which is expected to increase ten to a hundred times

in the coming decades (GEO5, 2012; Riegl et al., 2009). Extinction of marine species receives less

attention compared to extinction of terrestrial species (Riera et al., 2014), however, marine

ecosystems face considerable threats worldwide (White et al., 2006). Over exploitation, habitat loss,

pollution, global climate change and ocean acidification, as a result of carbon dioxide absorption by

the oceans, threaten the marine biosphere, resulting in a decrease in marine species biodiversity

(Dulvy et al., 2014; Gross, 2013).

Coral reef ecosystems are recognized as one of the most vulnerable marine ecosystems on the planet,

since coral reefs are highly sensitive to environmental changes (Gross, 2013). Coral reefs cover only

0.1% of the marine biosphere, but are home to a quarter to third of all marine fish species (Moberg &

Folke, 1999; Spalding et al., 2001). The diversity of coral and fish species is highest in the Coral Triangle

diversity hotspot, including eastern Indonesia, Sabah (Malaysia), Philippines, Papua New Guinea and

the Solomon Islands, covering 52% of the total species (Allen, 2008; Figure 1).

Figure 1: Location of the Coral Triangle diversity hotspot (obtained from Allen (2008)).

Although coral reefs are able to recover after severe damage (i.e. indicated by reef resilience), with

coral coverage, recruitment, diversity and community structure at the same levels as prior to the

damage (Gross, 2013), global climate change and anthropogenic disturbances are likely to reduce the

number and diversity of species depending on coral reefs. Especially species in diversity hotspots are

sensitive to these disturbances, since these species express high levels of habitat specialization, which

makes them extreme vulnerable to changes of their habitat (Holbrook et al., 2015).

Nowadays, 20% of all coral reefs worldwide are lost, another 50% of the coral reefs are in danger and

hardly any reef is not overfished (Riegl et al., 2009). Fisheries affect fish populations directly by

reducing abundance, size and biomass of target species (Fraser, 2013; Wilson et al., 2010), and

indirectly by habitat destruction and shifts in structure of fish communities (Wilson et al., 2010).

Species that have a juvenile stage of more than four years run the risk of local extinction if juveniles

are caught before reproducing. Depletion of these species from the foodweb may lead to the

6

expansion of a lower trophic level, for example algae, which might induce degradation of the whole

ecosystem (Gårdmark et al., 2015; Jouffray et al., 2015; White et al., 2006).

In order to protect coral reefs from overfishing, marine protected areas (MPAs) are created to increase

biotic and genetic diversity. The level of protection ranges from restrictions on catchment to whole

“no-take” areas. After establishment of a MPA, the condition of coral reef substrate improves with a

strong increase of living coral (White et al., 2006). Within these areas fish species have the chance to

become mature and increase their abundance, which in particular counts for target fish species

(García-Charton et al., 2004; White et al., 2006). As a result, the spawning stock of these species

increases and, hence, their reproduction rates (Fitzhugh et al., 2012; Hixon et al., 2014). Spillover of

larvae and migration of mature fish from the marine reserve to the non-reserve leads to improved

recruitment outside the reserve (Alcala, 2001; Harrison et al., 2012) and to improvement of the genetic

connectivity between the marine reserve and the non-reserve (Di Franco et al., 2012). However,

spillover and migration depend on trophic levels and fishing intensity, as high fishing intensity might

reduce abundance of certain fish families leading to increased abundance of species of lower trophic

levels (Ashworth & Ormond, 2004).

Connectivity between local populations through dispersal of larvae, juveniles or adults is key in

protection of meta-populations and resilience of species (Green et al., 2014), particularly for coral reef

fish species that use multiple habitats during their ontogenesis (Serafy et al., 2015). These shifts in

habitat use are assumed to be related to intraspecific predation and competition at the coral reef

habitat and to changes in reproductive status and diet as individuals become older (Mumby et al.,

2004). Mangroves and seagrass beds, for instance, provide nursery habitat for many juvenile fish,

which disperse to the coral reefs as sub-adult or adult (Mumby et al., 2004; Nagelkerken et al., 2000;

Serafy et al., 2015; Figure 2).

The presence of habitats suitable for juvenile fish (e.g. mangroves and seagrass beds) is found to

positively affect the community structure of coral reefs, abundance of fish species and biomass of fish,

Figure 2: Functions and exports of mutual benefits among mangroves, seagrass and coral reef ecosystems (obtained from

White et al. (2006)).

7

more than protection status of the reserve (Nagelkerken et al., 2012). It almost doubles the biomass

of community important fish that depend on these habitats, such as parrotfish, grunts and snappers

(Mumby et al., 2004). Absence of seagrass beds and mangroves, on the other hand, is found to reduce

density on coral reefs of species which depend on the nursery function of mangroves and seagrass

beds (i.e. nursery species) (Nagelkerken et al., 2002) and isolated reserves do not differ in fish

abundance from similar non-reserve coral areas (Olds et al., 2011). Therefore, coral reefs close to

mangrove and seagrass habitats are expected to harbour higher densities of adult fish of these species

than coral reefs at greater distance from these habitats (Dorenbosch et al., 2004a; Olds et al., 2011).

Besides functioning as a nursery habitat mangrove and seagrass beds also improve water quality by

stabilizing sediment, slowing down water movement and filtering freshwater from land (Björk et al.,

2008).

Since the Philippines are the centre of the Coral Triangle (Figure 1) (Honda et al., 2013), with the

highest concentration of species per unit area (Carpenter & Springer, 2005), the Philippines are the

front line of coral reef conservation. One of the first MPAs in the Philippines, Apo Island Marine

Sanctuary, was established in 1985 and is one of the world’s best examples of how MPAs can

contribute to improved reef fisheries management (White et al., 2006). Nowadays, over 1,000 MPAs

are established in the Philippines (985 MPAs in 2010 (Weeks et al., 2010); and, 1,557 MPAs according

to MPAtlas (2015)), with some community-based management successes. In general, fish density and

biomass improved with size and age of the MPA (Maliao et al., 2009). However, only 2.7 – 3.4% of the

MPAs are actual no-take zones and 90% of these areas are less than 1 km2 and thus, not suitable for

protection of large-bodied fish species. Nevertheless, since 70% of the MPAs is located within 5 km of

another reserve, the MPAs are well-spaced and might promote larval dispersal between MPAs (Weeks

et al., 2010).

The inclusion of habitats other than coral reefs within this network of MPAs is required to protect fish

species that depend on these habitats as a feeding or nursery habitat. However, only one study (Honda

et al., 2013) has compared the density and size of fish species among mangroves, seagrass beds and

coral reefs in the Philippines. This study confirmed that seven species used mangroves and/or seagrass

beds during their juvenile stage. Moreover, 37% of the commercial fish species was found in multiple

habitats, which emphasizes the importance of protection of mangrove and seagrass habitats.

This study aims to examine the research question; “What is the role of nursery habitats in the

effectiveness of marine protected areas?”, by determining the distances between a coral reef sanctuary

and mangrove and seagrass habitats, and their sizes, that stimulate dispersal of nursery fish species.

The study tests the hypotheses that (1) the diversity of nursery fish species on coral reefs increases

with increasing connectivity between reef and nursery habitat; (2) the diversity of nursery fish species

on coral reefs increases with increasing size of the nursery habitat; and, (3) the diversity of nursery fish

species on coral reefs is higher in MPAs than in non-MPAs. These hypotheses were tested by

monitoring selected fish species according to the belt-transect method in nine coral habitats, of which

four marine protected areas, of the municipalities Dauin, Zamboanguita and Siaton, Negros Oriental,

the Philippines. This study is a first step in determining the effect of size of nursery habitats and

distance between coral reefs and nursery habitats on fish life-ontogenetic migration. This knowledge

might result in an advice for management, considering protection and plantation of mangrove and

seagrass habitats near MPAs to conserve marine species diversity.

8

METHODS

STUDY SITE

This research was conducted under the leadership of Marine Conservation Philippines (MCP) which is

located in Zamboanguita, Negros Oriental, Visayas region, the Philippines (9°4’N; 123°9’E). The climate

of the research area is characterized by two winds: the Amihan from the North that rules from October

to the end of March and the Habagat from the South that dominates during the other half of the year.

Air temperatures range from 25°C to 35°C, with the hottest period beginning of May, whereas sea

temperature increases from 26°C in February to 30°C in summer. Annual total precipitation in the area

is approximately 1,700 mm, with most rain falling during the rainy season (mid-June until October)

(MCP, 2015).

SAMPLING DESIGN

This study focuses on nine coral reef areas of the coast of the municipalities Dauin, Zamboanguita and

Siaton of which four areas are MPAs (i.e. Andulay, Basak, Dauin Poblacion and Lutoban South). Eight

areas are located close to one of the four mangrove habitats (i.e. Lutoban river, Mayabon river, Siit

Bay and Tambobo Bay). Seagrass beds are located in front of eight of the coral reef areas (Table 1;

Figure 3).

Table 1: Site location, its conservation status, size (ha) and distance of the nearest mangrove and seagrass habitat (m).

# Site name MPA Mangroves Size (ha) Distance (m) Seagrass Size (ha) Distance (m)

1 Kookoo’s nest Non-MPA Tambobo bay 40,918 2,166 near Antulang 0.05 1,511

2 Antulang Non-MPA Siit bay 6,721 3,188 in front of reef 0.15 25

3 Andulay MPA Siit bay 6,721 1,980 in front of reef 0.01 106

4 Lutoban South MPA Lutoban river 5,932 455 in front of reef 15.34 22

5 Lutoban Pier Non-MPA Lutoban river 5,932 182 in front of reef 15.18 9

6 Guinsuan Non-MPA Mayabon river 15,468 4,174 in front of reef 1.83 15

7 Basak MPA Mayabon river 15,468 4,849 in front of reef 3.89 49

8 Malatapay Non-MPA Mayabon river 15,468 6,174 in front of reef 0.65 53

9 Dauin Poblacion MPA Mayabon river 15,468 15,336 in front of reef 0.13 33

The four reef locations (e.g. Dauin, Malatapay, Basak and Guinsuan) in the north differ from the reef

locations in the south. The reefs in the north face a stronger current, have a higher visibility, are more

patchy and the substrate surrounding the reef is sand, whereas the substrate at the other reefs consists

mostly of silt. This difference is caused by a strong current of the channel (Tañon straight) between the

islands Negros and Cebu, that flows from the north of Negros Oriental to the south. At the point of

Zamboanguita, the current flows land outwards and therefore leaves the reef locations in the south

unaffected.

9

Figure 3: Locations of the coral reef areas that were measured in this study. Numbers of sites correspond with the numbers in Table 1. Mangrove areas: a = Tambobo bay, b = Siit bay, c = Lutoban river, and d = Mayabon river. The Zamboanguita point is located just below coral reef area number 6.

NURSERY FISH SPECIES

Nursery reef fish species that use mangrove and/or seagrass habitat during their juvenile stage are

studied in various countries. A study in Bonaire, Netherlands Antilles (Nagelkerken et al., 2000), found

that of the 16 species selected, five fish species used seagrass beds as nursery habitat, whereas four

species used mangrove forest as nursery habitat. In Japan, among the 319 species recorded, four fish

species used seagrass beds as nursery habitat during their juvenile stage, whereas three fish species

used mangrove habitats (Shibuno et al., 2008).

In the Philippines abundance of fish species recorded in coral reefs was higher (234 species) than in

seagrass beds (38 species) and mangrove forest (47 species). Fourteen percent of the species used

multiple habitats, of which six species used both coral reefs and seagrass habitats, nine species used

both coral reefs and mangrove habitats and eight species used all three habitats. Seven fish species

used mangrove and/or seagrass habitats during their early ontogenetic stage, of which six species were

commercial important species (Honda et al., 2013).

10

Since this study focuses on fish life-ontogenetic migration, only reef fish species of families that are

expected to use different habitats during their ontogenesis were taken into account to examine the

importance of connectivity and size of nursery habitats. Additionally, specialization on a subset of fish

species was expected to improve detectability of fish species during field measures, since observers

become familiar with the selected species, and, hence, will improve the reliability of the data.

The fish species that were recorded in multiple habitats by studies in the Indo-Pacific region

(Dorenbosch et al., 2004b; Dorenbosch et al., 2005; Honda et al., 2013; Igulu et al., 2014; Kimirei et al.,

2013; Nagelkerken et al., 2000; Nakamura et al., 2008; Shibuno et al., 2008) and that were known to

occur at the reef locations based on the Baseline Study performed by MCP, were selected. The list

consisted of 34 fish species of the families Lutjanidae, Haemulidae, Nemipteridae, Lethrinidae,

Mullidae, Labridae, Scaridae, Siganidae and Sphyraenidae (Appendix I).

FISH MONITORING

Fish monitoring methods vary from determining the density of target species to monitoring fish

spawning aggregation and fish recruitment. The belt transect method is most suitable for this study

considering the goal of examining densities of target fish species. Although the fish belt transect

method is susceptible to double-counting of individuals, since fish move along the transect and might

respond on the movement of divers, it is more suitable for this type of study since it is easily usable by

volunteer divers (Hill & Wilkinson, 2004) and is already used as permanent measuring method by

Marine Conservation Philippines. In addition, transects of 20 m are also used by Honda et al. (2013)

that also observed habitat use of reef fishes in the Philippines.

The Reef Check method uses a belt transect of 5 m x 100 m and 5 m high, consisting of four sections

of 20 m each with 5 m gaps in between. Fifteen minutes after establishing the transect, to minimize

fish disturbance, the observers swim slowly at each side of the transect line and stop every 5 m to

count the number of adult fishes of the selected species, with a pause of 1 minute at each 5 m stop

point. The fifth, tenth and fifteenth stop point were skipped to start with a new 20 m section of the

transect. In total, thus, four replicates of 20 m each with a total survey length of 80 m were measured.

At each reef location, two transect lines of 100 m were established, one at a depth of 4 – 6 m and the

other at 10 – 12 m. Each transect was measured five times during the period end-February until end-

May 2016. This has resulted in 20 samples per transect and, thus, a total sample size of 360 samples.

The fish surveys occurred between 8:30 and 16:30h.

MANGROVE AND SEAGRASS HABITAT MAPPING

Mangroves of Lutoban river, Mayabon river, Siit Bay and Tambobo Bay were mapped by walking along

the edge of the mangrove forest, using a GPS to record the track. At each reef site, seagrass beds were

mapped based on percentage cover, which was estimated in quadrats of 25 cm x 25 cm. Only cover of

more than 20%, according to the Seagrass-Watch monitoring protocols percent cover standards

(McKenzie et al., 2003), was considered as suitable for juvenile nursery fish. Seagrass beds were

mapped by snorkelling along the edge of seagrass beds with a coverage of more than 20% per 25-

quadrat, with a GPS recording the track.

Based on the mapping, the size of mangrove and seagrass habitats and distance from the transect to

the habitats was calculated using QGIS 2.14. The buffer tool and measure line tool were used to

determine habitat size and distance to the reef transect (Table 1). Nursery habitats located up to 500

11

m from the transect lines were included to calculate the size of nursery habitats. This measure was

based on the linear scale of movement of coral reef fish species of Green et al. (2015). According to

this scale, larvae of most of the selected nursery species disperse up to 500 m (e.g. species of the

families Lutjanidae, Haemulidae, Ephinephelus) from their nursery habitat.

DATA ANALYSIS

A Kruskal-Wallis and a subsequent Dunn’s post-hoc test with Bonferroni adjustment was used to

compare the number of nursery species among the different reef locations. A logistic Generalized

Linear Model was used to indicate the chance a species is present on the reef locations. Presence per

nursery fish species (presence/sample) was used as dependent variable and was related to the

independent variables: distance to nearest mangrove forest (m), distance to nearest seagrass bed (m),

size of nearest mangrove forest (ha), size of nearest seagrass bed (ha), depth (5 vs. 10 m), conservation

status of reef area (MPA vs. non-MPA) and geographical location (north vs. south).

A Generalized Linear Model (GLM) with Poisson distribution was used to quantify the relationship

between abundance of nursery fish species and the size and connectivity with nursery habitat(s). The

dependent variable was abundance per present nursery fish species (n/sample) and the independent

variables were the same as for the logistic regression.

Although the residuals of the logistic regression on species presence were not normally distributed,

nursery habitat was assumed to be important for the species that were significantly related to nursery

habitat(s). For this subset of species, species richness and Shannon-Wiener diversity index (Equation

1) were calculated using the vegan package of R. The Shannon-Wiener index takes into account species

richness and the proportion of each species within the community, based on the number of individuals

per species (pi) in the sample (Spellerberg, 2008). A GLM was used to quantify the relationship between

species richness and diversity of nursery species (index) and the different independent variables as

previously described. A likelihood ratio test was performed to determine the best fitting model.

(1) 𝐻′ = − ∑ 𝑝𝑖 ln 𝑝𝑖

𝑅

𝑖=1

12

RESULTS

In total, 31 nursery fish species were observed on the reef transects. The highest number of nursery

fish species was observed in Basak and the lowest number in Andulay, both MPAs. The highest number

of individual nursery fish was observed in Basak, whereas the lowest number of individuals was

observed in Kookoo’s nest (Figure 4). The distance from the coral reef areas to mangrove forests

ranged from 183 to 15,336 m and from coral reefs to seagrass beds from 9 to 1,511 m. The size of

mangrove forests ranged from 5,932 to 40,918 ha and the size of seagrass beds from 0.01 to 15 ha.

Thus, both the independent variables as the dependent variables varied strongly among the locations.

Figure 4: Number of nursery fish species and number of individual nursery fish observed per reef location. The dark-blue reef locations are MPAs, whereas the light-blue reef locations are non-MPAs. The letters represent the results of the Kruskal-Wallis test with Dunn post-hoc and Bonferonni adjustment method (X2 = 67.83, p < 0.001): locations with the same letter do not significantly differ (p > 0.05) in number of nursery fish species observed.

The number of nursery fish species (n/sample) differed among the reef locations (Kruskal-Wallis Dunn

post-hoc and Bonferonni adjustment method: X2 = 67.83, p < 0.001). This indicates that there is a

varying external factor determining the presence and abundance of nursery fish species on the reef

locations, which was investigated further with the GLMs.

FISH SPECIES PRESENCE

Twenty-one fish species were significantly affected by the size of nursery habitats, distance to seagrass

habitat and/or distance to mangrove forest (log). Additionally, two fish species were significantly

affected by an interaction of these variables with depth (logistic regression: p < 0.05; Table 2). Although

none of the residuals were normally distributed, the significant relationships suggest that nursery

habitats might be important for the selected fish species.

bcd

cd

bd

cd

bcd

c

bcd

ab

a

0 5 10 15 20 25

Andulay

Antulang

Lutoban South

Kookoo's nest

Malatapay

Lutoban Pier

Guinsuan

Dauin Poblacion

Basak

Number of nursery fish species observed

0 200 400 600 800 1000 1200

Number of individual nursery fish observed

13

Table 2: Logistic Generalized Linear Model of the relationships between the presence of nursery fish species and distance to nearest mangrove forest (m), distance to nearest seagrass bed (m), size of nearest mangrove forest (ha), size of nearest seagrass bed (ha), depth (5 vs. 10 m), conservation status of reef area (MPA vs. non-MPA) and geographical location (north vs. south). For the species that were only significant related to an interaction of the previous described variables, the significance of these interactions were shown.

Independent variables Ab

ud

efd

uf

sexf

asc

iatu

s

Ab

ud

efd

uf

vaig

ien

sis

Ch

eilin

us

chlo

rou

rus

Ch

eilo

dip

teru

s q

uin

qu

elin

eatu

s

Epin

eph

elu

s m

erra

Fist

ula

ria

co

mm

erso

nii

Ha

lich

oer

es a

rgu

s

Ha

lich

oer

es h

ort

ula

nu

s

Ha

lich

oer

es s

cap

ula

ris

Leth

rin

us

ha

rak

Leth

rin

us

ob

sole

tus

Lutj

an

us

dec

uss

atu

s

Lutj

an

us

ehre

nb

erg

ii

Lutj

an

us

fulv

ifla

mm

a

Lutj

an

us

fulv

us

Lutj

an

us

gib

bu

s

Lutj

an

us

mo

no

stig

ma

Mu

lloid

ich

thys

fla

volin

eatu

s

Pa

rup

eneu

s b

arb

erin

oid

es

Pa

rup

eneu

s b

arb

erin

us

Sca

rus

psit

tacu

s

Sco

lop

sis

bili

nea

ta

Sig

an

us

spin

us

Stet

ho

julis

tri

linea

ta

Distance to seagrass (m) *** *** *** *** *** *** *** * *** *** *** *** *** *** *** *** *** *** *** *** ***

Size seagrass (ha) *** *** *** *** *** *** *** ** *** *** *** *** *** *** *** *** *** *** *** *** ***

Distance to mangroves (m, log) *** *** *** *** *** *** *** ** *** *** *** *** *** *** *** *** *** *** *** * *** ***

Size mangroves (ha) *** *** *** *** *** *** *** *** *** *** *** *** *** *** *** *** *** *** *** ***

Depth (ref = 5 m) *** *** *** *** *** *** *** *** *** *** *** *** *** *** *** *** *** *** *** ***

Conservation status (ref = MPA) *** *** *** *** *** *** *** *** *** *** *** *** *** *** *** *** *** *** *** ***

Geographical location (ref = north) *** *** *** *** *** *** *** *** *** *** *** *** *** *** *** *** *** *** *** ***

Distance seagrass : size seagrass *

Size seagrass : depth ***

Distance mangroves(log) : depth ***

Size mangroves : depth **

Conservation status : depth *

Depth : geographical location *

*P < 0.05; **P < 0.01; ***P < 0.001; empty, not significant (P > 0.05)

14

Table 3: Generalized Linear Model of the relationships between the abundance of present nursery fish species and distance to nearest mangrove forest (m), distance to nearest seagrass bed (m), size of nearest mangrove forest (ha), size of nearest seagrass bed (ha), depth (5 vs. 10 m), conservation status of reef area (MPA vs. non-MPA), geographical location (north vs. south) and interactions of these variables.

Independent variables Ab

ud

efd

uf

sexf

asc

iatu

s

Ab

ud

efd

uf

vaig

ien

sis

Ch

eilio

iner

mis

Ch

eilo

dip

teru

s q

uin

qu

elin

eatu

s

Ha

lich

oer

es h

ort

ula

nu

s

Lutj

an

us

fulv

ifla

mm

a

Mu

lloid

ich

thys

fla

volin

eatu

s

Pa

rup

eneu

s b

arb

erin

oid

es

Pa

rup

eneu

s b

arb

erin

us

Sco

lop

sis

bili

nea

ta

Sco

lop

sis

cilia

ta

Distance to seagrass (m, log) *** *** * * *** *

Size seagrass (ha, log) * ** *** * *

Distance to mangroves (m) ** *** ** *

Size mangroves (ha) *** ** **

Depth (ref = 5 m) *** ** ***

Conservation status (ref = MPA) ** *** *

Geographical location (ref = north) ** ** *** *

Distance seagrass(log) : size seagrass ** ** *

Distance seagrass(log) : size mangroves **

Distance seagrass(log) : depth *** ***

Size seagrass : depth ** **

Distance mangroves : depth ***

Size mangroves : depth *

Distance seagrass(log) : size seagrass : depth **

*P < 0.05; **P < 0.01; ***P < 0.001; empty, not significant (P > 0.05)

FISH ABUNDANCE

Eight fish species were significantly affected by size of nursery habitats, distance to nearest seagrass

habitat (log) and/or distance to the nearest mangrove habitat. Additionally, two fish species were

significantly affected by an interaction of these variables with depth (general linear model: p < 0.05;

Table 3). Although none of the residuals were normally distributed, the significant relationships

suggest that nursery habitats might be important for the selected fish species.

FISH SPECIES DIVERSITY

Species richness and diversity of nursery species was based on the 21 fish species that were

significantly related to size and/or distance to the nearest nursery habitat, according to the logistic

regression (Table 2). Diversity was positively related to size of mangrove forests and conservation

status of the reef area, whereas it was negatively related to distance to the nearest mangrove forest

and size of seagrass beds (Table 4). This model fitted the data significantly better than the alternative

model (likelihood test = p < 0.001), however the residuals were not normally distributed.

15

Table 4: Generalized Linear Model of the relationships between the Shannon-Wiener diversity index and distance to nearest mangrove forest (m), distance to nearest seagrass bed (m), size of nearest mangrove forest (ha), size of nearest seagrass bed (ha), depth (5 vs. 10 m), conservation status of reef area (MPA vs. non-MPA) and geographical location (north vs. south).

Independent variables Estimate Standard Error t-value

Constant - 10.42 * 4.707 - 2.214

Distance to seagrass (m, log) 1.271 1.333 0.953

Size of seagrass bed (ha, log) - 3.408 * 1.638 - 2.080

Distance to mangroves (m, log) - 2.242 * 1.009 - 2.223

Size of mangrove forest (ha, log) 3.108 * 1.333 2.332

Depth (ref = 5m) - 3.278e+12 9.859e+12 - 0.332

Conservation status (ref = MPA) - 0.4065 *** 0.09155 - 4.440

Geographical location (ref = north) - 0.4617 0.7299 - 0.632

*P < 0.05; **P < 0.01; ***P < 0.001; others, not significant (P > 0.05)

Species richness of nursery species was positively related to size of mangrove forest and conservation

status of the reef area, whereas it was negatively related to distance to mangrove forest and size of

seagrass bed (Table 5). This model fitted the data significantly better than the alternative model

(likelihood test = p < 0.001), however the residuals were not normally distributed.

Table 5: Generalized Linear Model of the relationships between species richness of nursery species and distance to nearest mangrove forest (m), distance to nearest seagrass bed (m), size of nearest mangrove forest (ha), size of nearest seagrass bed (ha), depth (5 vs. 10 m), conservation status of reef area (MPA vs. non-MPA) and geographical location (north vs. south).

Independent variables Estimate Standard Error t-value

Constant - 41.069 ** 14.35 - 2.905

Distance to seagrass (m, log) 6.022 4.064 1.482

Size of seagrass bed (ha, log) - 13.79 ** 4.996 - 2.760

Distance to mangroves (m, log) - 8.951 ** 3.076 - 2.910

Size of mangrove forest (ha, log) 12.45 *** 4.064 3.063

Depth (ref = 5m) - 1.028e+13 3.006e+13 - 0.342

Conservation status (ref = MPA) - 1.427 *** 0.2791 - 5.111

Geographical location (ref = north) - 2.680 2.226 - 1.204

*P < 0.05; **P < 0.01; ***P < 0.001; others, not significant (P > 0.05)

16

DISCUSSION

This study indicated the importance of nursery habitats (i.e. mangrove forests and seagrass beds) to

support fish migration in Negros Oriental, Philippines. Even though the non-normal distribution of the

model residuals of all models suggests that other factors that were not measured in this study play an

important role in presence, diversity and abundance of our species, the results do suggest that

presence and abundance of nursery fish species on the coral reefs are related to size and connectivity

of both mangrove forests and seagrass beds. The size of mangrove forest, connectivity with mangrove

forest and conservation status were key in determining nursery fish species diversity (Shannon-Wiener

index) and species richness of nursery fish species. Size of seagrass beds, on the other hand, negatively

affected fish species diversity and species richness of nursery fish species, which is in disagreement

with our predictions. These results indicate the importance of size and connectivity of mangrove forest

for nursery fish species and, hence, reef fish communities in the Philippines. Protection and

replantation of mangrove forest near coral reefs, specifically marine protected areas, should be

obtained in management protocols in order to conserve marine species diversity.

FISH SPECIES PRESENCE AND ABUNDANCE

Presence of 62% and abundance of 24% of the selected nursery fish species was significantly affected

by size and connectivity of mangrove forests and seagrass beds. Presence of most of the fish species

was highly significant related to all four nursery habitat variables, whereas Scolopsis bilineata was only

related to distance to mangroves, and Halichoeres scapularis to size of seagrass beds and distance to

seagrass and mangrove areas. This is remarkable since S. bilineata nurses in seagrass beds and H.

scapularis in mangroves, according to literature (Honda et al., 2013). One explanation for this

difference might be that these species are opportunistic in nursery habitat use, depending on food

availability (Nakamura et al., 2012; Newman et al., 2012), and might even use coral reefs as alternative

nursery habitat (Dorenbosch et al., 2004a; pers. obs.). Difference in food availability between study

areas might therefore result in differences in nursery habitat use for these species, nevertheless, it still

indicates the importance of nursery habitats for these species. Thus, although the presence of some

of the fish species seems to be determined by another type of nursery habitat than predicted, it

suggests that nursery habitats determine the presence of most of the selected nursery fish species.

Density of seven fish species was related to size and/or connectivity of nursery habitats. Abudefduf

sexfasciatus and Lutjanus fulviflamma were related to size of seagrass beds only, whereas A. vaigiensis

and Cheilodipterus quinquelineatus were related to size and connectivity of both mangrove and

seagrass areas. This is remarkable since both species of Abudefduf nurse in mangrove areas (Honda et

al., 2013), whereas L. fulviflamma nurses in both seagrass and mangrove areas (Honda et al., 2013;

Igulu et al., 2014; Kimirei et al., 2013; Shibuno et al., 2008). Halichoeres hortulanus, Mulloidichthys

flavolineatus and Parupeneus barberinus were related to both mangrove forest and seagrass beds,

however, M. flavolineatus and H. hortulanus nurses in seagrass beds (Honda et al., 2013). Parupeneus

barberinoides, on the other hand, was related to connectivity with seagrass beds. Cheilio inermis and

Scolopsis ciliata were not related to nursery habitats, only to depth. However, both species nurse in

either seagrass or mangrove areas, respectively (Honda et al., 2013). These differences in nursery

habitat use might be explained by opportunistic habitat use based on food availability (Dorenbosch et

al., 2004a; Nakamura et al., 2012; Newman et al., 2012). Thus, although some species are related to

17

another type of nursery habitat than predicted, nursery habitats seem to determine the density of

some of the selected nursery fish species.

Nine out of 21 species (43%), which presence was related to nursery habitats, and three out of seven

species (43%), which density was related to nursery habitats, were commercial important fish species

(Honda et al., 2013). For presence this concerned the species Epinephelus merra, Lethrinus harak,

Lutjanus decussatus, L. fulvus, L. monostigma and Scarus psittacus, and for both presence and

abundance the species L. fulviflamma, Mulloidichthys flavolineatus and Parupeneus barberinoides.

Other studies confirm that species that exhibit ontogenetic shifts and species that migrate between

habitats have fishery value (Kimirei et al., 2011; Lugendo et al., 2005; Mumby et al., 2004; Nagelkerken

et al., 2000). This emphasizes the importance of conserving mangrove and seagrass areas, especially

near marine protected areas, to promote the reproductive success of commercially important fish and,

hence, sustainable fishery by local fishermen.

FISH SPECIES DIVERSITY

I hypothesized that fish species diversity would increase with increasing connectivity between reef and

nursery habitat, increasing size of nursery habitat and conservation status of the reef area. Based on

the 21 fish species that were related to seagrass or mangrove areas, the Shannon-Wiener diversity

index and number of fish species were calculated. Both the diversity index and species richness of

nursery fish species increased with increasing connectivity between reef area and mangrove forest,

size of mangrove forest and strongly with conservation status of the reef area. These findings are

consistent with the findings of other studies focused on the effect of mangrove forests (Dorenbosch

et al., 2004a, 2005, 2007; Mumby et al., 2004; Nagelkerken et al., 2000, 2001, 2002), size of mangrove

forests (Serafy et al., 2015) and conservation status on nursery fish species (Olds et al., 2011). The

effect of mangrove forest on nursery fish species is an important finding for future management of

marine ecosystems, particularly since the effect of mangrove forests might even overrule the effect of

conservation status on structure and abundance of reef fish (Nagelkerken et al., 2012). Thus, both size

and connectivity of mangrove forest and conservation of the reef area determine nursery fish species

diversity and, hence, reef fish communities.

In contrast to this hypothesis, size of seagrass beds negatively affects both the diversity index and

species richness of nursery fish species. This is surprising, since seagrass beds are suggested to increase

nursery fish species density and diversity (Dorenbosch et al., 2004a; Honda et al. 2013; Nagelkerken et

al., 2000, 2012). One explanation for these contradictory findings might be that large seagrass beds

were specifically found in front of fishermen village and are not included in no-take zones, which might

cause a reversed effect.

STRENGTHS AND LIMITATIONS OF THE STUDY

This study is unique as it considers possible effects of size and connectivity of seagrass and mangrove

areas on presence, density and diversity of nursery fish species, and provides more information about

conservation of reef fish communities in the Philippines. A large range in size of seagrass beds (0.01-

15 ha) and mangrove forests (5,932-40,918 ha) and a large sample size (360 samples) was used, which

should be sufficient to gain clear and strong results. Another study on nursery fish species in the

Philippines was focused on habitat use of different fish species, while this study tried to indicate the

effect of size and distance of nursery habitats on reef fish communities.

18

The methods used in this study to determine fish species diversity and the size and connectivity of

nursery habitats were likely sufficient to find answers to the hypotheses. However, fish species were

only recorded during the dry season in the months February to May, which might affect the results.

Furthermore, other factors, such as reef type, patchiness, turbidity and soft substrate type (sand versus

silt) might influence the data and was not included in this study. Additionally, I tracked seagrass beds

by snorkelling around the edge of the bed, without distinguishing between different species of

seagrass. However, different species of seagrass might provide nursery habitat for specific fish species

and this might affect the results.

One reason for the differences between the results of this study and other literature might be that the

presence of nursery fish species and density of nursery fish species are not adequate to indicate

nursery habitat-use of fish. Furthermore, I only recorded the number of adult fish on coral reefs,

whereas other studies (e.g. Honda et al., 2013; Nagelkerken et al., 2000) also recorded individual

juvenile fish within nursery habitats in order to predict if the fish species undergo an ontogenetic shift

in habitat. However, the fish species selected for this study were determined as nursery fish species

by literature, therefore, the results from this study are likely to account for both migration between

habitats and life-ontogenetic shifts (Nagelkerken et al., 2012). Nevertheless, since fish species were

only recorded on coral reefs, species that only occur in mangrove or seagrass habitats were not

recorded, although these fish species are less flexible in habitat use and therefore are more dependent

on these habitats than nursery reef species that use multiple habitats (Honda et al., 2013).

PRACTICAL IMPLICATIONS FOR MARINE CONSERVATION

The fish species diversity index and species richness of nursery fish species increased with increasing

connectivity between reef area and mangrove forest, size of mangrove forest and conservation status

of the reef area. This is an important finding, since mangrove forest face strong reduction in the

Philippines due to harvesting of trees (Primavera, 2000; Valiela et al., 2001). Since fish species that

migrate to mangrove areas use both natural and transplanted mangrove areas (Honda et al., 2013),

replantation of mangrove forest and inclusion of transplanted and natural mangrove forest in the

marine protected area could be considered to promote recovery of reef fish communities.

Protection and replantation of mangrove forest is expected to lead to higher catch rates for fishermen,

as 43% of the fish species that depend on connectivity and size of mangrove habitat have fishery value.

Especially an increase in larger individuals of commercial important species is expected when

mangrove forests are replanted close to marine protected areas (Nagelkerke et al., 2012). Aside of

increased sustainability of fishery resources, mangroves furthermore provide a buffer against storms

(Alongi, 2008) and fix carbon (Bouillion et al., 2008; Donato et al., 2011). This highlights the overall

importance of mangrove forest replantation for the local community.

RECOMMENDATIONS FOR FUTURE RESEARCH

This study highlights that a better understanding of the mechanisms behind reef fish communities in

the Philippines is of crucial importance for both the marine ecosystem and the fishermen community.

The results do indicate a strong relationship between nursery fish species and nursery habitat, but the

residuals were not normally distributed. The non-normality of the residuals suggests that other factors,

such as reef type and substrate, might influence nursery fish species aside of nursery habitat, depth,

conservation status and geographical location. Since reef type, patchiness, turbidity and substrate

19

differ strongly among the nine areas studied, a similar study on the reef areas of the island Siquijor,

close to Negros, could be considered, since these reef areas are more similar to each other.

Future studies on nursery fish species should consider to measure fish abundance and structure year-

round, since this will provide more information on fish migration, as both the dry and wet season is

included. Furthermore, transects on a depth of 16 – 18 m could be considered, since some fish species

prefer deeper reefs as adult. Other habitat characteristics, such as seagrass species, mangrove species,

distance to river and fishing intensity, could be considered, since these factors might affect fish species

density and diversity. More research will provide better insight in the complex relationship between

nursery habitat and reef fish communities, and implications for conservation of the marine ecosystem

in the southern part of Negros Oriental.

CONCLUSION

This study suggests that the diversity of nursery reef fish species in the Philippines increases with

increasing connectivity between reef area and mangrove forest, increasing size of mangrove area and

conservation status of the reef area. More than two-fifth of the fish species affected by connectivity

and size of mangrove forest are important reef community species with fishery value for fishermen.

Furthermore, marine protected areas seem indeed to contribute to the structure and abundance of

reef fish communities. These findings emphasizes the importance to protect coral reefs and replant

mangrove forests in order to promote reef fish communities and local fishery resources.

20

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APPENDIX I: SELECTED FISH SPECIES

Table I: Selected fish species monitored during this research. Selection is based on the use of multiple habitats (i.e. coral reefs and nursery habitat(s)), the nursery habitats (i.e. mangrove and/or seagrass habitat) the fish species uses and the study recording.

Nursery fish species Nursery habitat Study

Fistulariidae

Fistularia commersonii Mangrove Honda et al., 2013

Serranidae

Epinephelus merra Seagrass Honda et al., 2013

Apogonidae

Cheilodipterus quinquelineatus Seagrass & Mangrove Honda et al., 2013

Lutjanidae

Lutjanus decussatus Mangrove Honda et al., 2013

Lutjanus ehrenbergii Seagrass Dorenbosch et al., 2004b

Lutjanus fulviflamma Seagrass & Mangrove Honda et al., 2013; Igulu et al., 2014; Kimirei et al., 2013; Shibuno et al., 2008

Lutjanus fulvus Seagrass & Mangrove Honda et al., 2013; Nakamura et al., 2008; Shibuno et al., 2008

Lutjanus gibbus Seagrass Shibuno et al., 2008

Lutjanus monostigma Seagrass & Mangrove Dorenbosch et al., 2005; Honda et al., 2013; Igulu et al., 2014; Shibuno et al., 2008

Haemulidae

Plectorhinchus flavomaculatus Seagrass Dorenbosch et al., 2005

Plectorhinchus lineatus Mangrove Honda et al., 2013

Nemipteridae

Scolopsis bilineata Mangrove Honda et al., 2013

Scolopsis ciliata Mangrove Honda et al., 2013

Lethrinidae

Lethrinus harak Seagrass & Mangrove Honda et al., 2013; Kimirei et al., 2013

Lethrinus microdon Seagrass & Mangrove Igulu et al., 2014

Lethrinus obsoletus Seagrass Shibuno et al., 2008

Mullidae

Parupeneus barberinoides Seagrass Shibuno et al., 2008

Parupeneus barberinus Seagrass & Mangrove Honda et al., 2013

Mulloidichthys flavolineatus Seagrass Dorenbosch et al., 2005; Igulu et al., 2014

Pomacentridae

Abudefduf lorenzi Mangrove Honda et al., 2013

Abudefduf sexfasciatus Mangrove Honda et al., 2013

Abudefduf vaigiensis Mangrove Honda et al., 2013

Labridae

Cheilinus chlorourus Seagrass Honda et al., 2013

Cheilinus undulatus Seagrass & Mangrove Dorenbosch et al., 2005; Igulu et al., 2014

Cheilio inermis Seagrass Honda et al., 2013

Halichoeres argus Seagrass & Mangrove Honda et al., 2013

Halichoeres hortulanus Seagrass Honda et al., 2013

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Halichoeres scapularis Seagrass & Mangrove Honda et al., 2013

Stethojulis trilineata Seagrass & Mangrove Honda et al., 2013

Scaridae

Scarus psittacus Seagrass & Mangrove Dorenbosch et al., 2005

Siganidae

Siganus guttatus Mangrove Honda et al., 2013

Siganus spinus Seagrass & Mangrove Honda et al., 2013

Siganus virgatus Mangrove Honda et al., 2013

Sphyraenidae

Sphyraena barracuda Seagrass & Mangrove Honda et al., 2013; Nagelkerken et al., 2000