Community structure of copepods from different nearshore substrates off Tinggi and

Sibu Islands, Malaysia*Ephrime B. Metillo1, Shuhei Nishida2, Othman BH Ross3, Fatimah Md.

Yusof4, Susumu Ohtsuka5, Mulyadi6, Shozo Sawamoto7, Jun Nishikawa2, Hideo Sekiguchi8, Tatsuki Toda9, Nozomu Iwasaki10,

Tomohiko Kikuchi11, Nguyen Thi Thu12, Nguyen Cho13, Khwanruan Srinui14, Wilfredo Campos15

1Department of Biological Sciences, Mindanao State University-Iligan Institute of Technology, Iligan 9200, Philippines

2Atmosphere and Ocean Research Institute, University of Tokyo, Kashiwanoha 5-1-5, Kashiwa 277-8564 Japan

3Marine Ecosystem Research Centre, Faculty of Science & Technology, Universiti Kebangsaan Malaysia, 43600 UKM Bangi, Malaysia

(Addresses of other authors are in appendices)

*Paper presented in Census of Marine Zooplankton (CMARZ) Regional Symposium for Asia, Institute of Oceanography of the Chinese Academy of Science (IOCAS), Qingdao, China 11-14 May 2010

Copepods dominate most tropical zooplankton samples; have pivotal role in bentho-pelagic food webs and ecosystems and fisheries

Few studies on tropical copepods despite their sensitivity to climate change and water pollution

Dearth of information on community structure of tropical copepods

Japan Society for the Promotion of Science (JSPS)Zooplankton Biodiversity Research Group for Southeast Asia (2004-2010) - an internationalcollaborative team focusing on zooplankton in Southeast Asian waters

GOAL AND OBJECTIVES

Under an umbrella goal of developing a standard monitoring system for the coastal waters of Southeast Asia using copepod communities, this study was specifically aimed to:

1. identify copepod species from small and large fractions of samples that make up communities from coral, seagrass and sand substrates;

2. analyze the structure of copepod communities using univariate diversity indices and rank-dominance technique and constrained multivariate ordination method

3. identify indicator species and assemblage of species using Dufrene and Legendre (1997) indicator value index

MalaysiaPeninsula

Southeast Asia

Pacific Ocean

STUDY SITES

MalaysiaPeninsula

Tinggi Island

Sibu Island

Sibu IslandCoral area

200 m

offshore

inshore

Sibu IslandSandy area 200 m

inshore offshore

Tinggi IslandSeagrass bed

200 m

inshoreoffshore

SITES (Coral, Seagrass, Sand)

TIME: DAY (10:00, 12:00, 14:00)NIGHT (19:00, 21:00, 23:00)

STATIONS (Inshore, Offshore)

ZOOPLANKTON SAMPLING AND SORTING

1 m

2-kg sinker

Vertical tow of 100-µm net

cod end

flow meter

SPECIES1 2 3 4

SA

MP

LE

S CANONICAL CORRESPONDENCE ANALYSIS: Eigenvalues, Monte Carlo Permutations,Forward Selection

-1.0 0.4

-0.8

0.8

CycloCalan

Harpa

Decap

OstraLarva

Salps

Antho

Polyc

ChaetPyros

FishLar

Auricu

Bipinn

Zoea

Megal

BivelGasvelCopepCopNau

Ophiop

Echin

FishEgg

Barcy

TintinForam

Temp

pH

Salinity

SecchiD

TSS

DO

NO2

PO4CHLa

Canonical Community Ordination (CANOCO) Analysis Stages

PRIMER-E v.5 Multivariate Analysis Stages

SAMPLES1 2 3 4

SP

EC

IES

Transformed (to balance rarer and common species)

Community Parameters (per sample)

Shannon Species Diversity Index

Pielou’s Evenness Index

Number of species

Number of individuals

K-dominance curves

IndValij = Aij X Bij X 100, where

Aij = Nindividualsij/Nindividualsj (Aij, a measure of specificity; Nindividualsij, is the mean number of individuals of species i across sites of group j; Nindividualsj, is the sum of the mean numbers of individuals of species i over all groups)

Bij = Nsitesij/Nsitesj (Bij, a measure of fidelity; Nsitesij is the number of sites in

cluster j where species i is present; Nsitesj, is the total number of sites in that cluster. Bij is maximum when species i is present in all objects of cluster j)

INDICATOR SPECIES AND ASSEMBLAGE OF SPECIES

Dufrene and Legendre (1997) Indicator Value (IndValij) Index

Current velocity and direction measured by ADCP at the nearshore waters off Tinggi and Sibu Islands. Currents shown in A were recorded during ebb tide and those in B during flood tide.

Tim

e

2o 08’ N

2o 18’ N

2o 23’ N

103o 52’ E 104o 04’ E 104o 12’ E

Tinggi Is.

MalaysiaPeninsula

Sibu Is.

N

5 Km

BT

ime

(min

)

2o 08’ N

2o 18’ N

2o 23’ N

103o 52’ E 104o 04’ E 104o 12’ E

Tinggi Is.

MalaysiaPeninsula

N

5 Km

A

Sibu Is.

Temperature (oC), salinity (‰) and dissolved oxygen (mg L-1) measured at coral (A), seagrass (B), and sand (C) sites. Left y-axis – temperature and salinity; right y-axis – dissolved oxygen.

27.0

28.0

29.0

30.0

31.0

32.0

33.0

34.0

D1C1 D1C2 N1C1 N1C2 D2C1 D2C2 N2C1 N2C2 D1CO1D1CO2 N1CO1N1CO2 D2CO1D2CO2 N1CO1N1CO20

1

23

4

5

6

7

8

9

10

27.0

28.0

29.0

30.0

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D1G1 D1G2 N1G1 N1G2 D2G1 D2G2 N2G1 N2G2 D1GO1D1GO2 N1GO1N1GO2 D2GO1D2GO2 N2GO1N2GO2012

3

4

56

7

89

10

27.0

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29.0

30.0

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D1S1 D1S2 N1S1 N1S2 D2S1 D2S2 N2S1 N2S2 D1SO1D1SO2 N1SO1N1SO2 D2SO1D2SO2 N2SO1N2SO20

12

3

4

56

7

89

10

A

B

C

coral

seagrass

sand

TEMP: differed between sites andtime, not between stations – elevated values at sand site andin the afternoon

SAL: varied between sites, but not between stations and time –highest from sand site

DO: varied between sites and time, not between stations – widest range at seagrass site

100-335 µm copepods

Oithona decipiens

Kelleria sp.

Macrosetella gracilis

Oithona plumifera

Acartia pacifica

Oithona attenuata

Paracalanus aculeatus

Sapphirella-type

Acrocalanus gibber

Bestiolina similis

Clytemnestra scuttelata

Euterpina acutifrons

Metacalanus sp.

Metis sp.Microsetella norvegica

Oithona nana

Oithona rigida

Oithona simplex

Paracalanus parvusParvocalanus crassirostris

Parvocalanus elegans

Pseudocyclops sp.

24 species (5 unique)

Harpacticoida

Cyclopoida

Calanoida

Poicilostomatoida

Corycaeus spp.Oncaea spp.

> 335 µm copepods 66 species (42 unique)

Acrocalanus gracilis

Centropages orsini

Clytemnestra scutellata

Corycaeus andrewsi

Corycaeus dahli

Eudactylopus latipes

Euterpina acutifrons

Kelleria sp.

Macrosetella gracilisMetacalanus aurivilli

Microsetella norvegica

Oithona attenuataOithona decipiensOithona nanaOithona oculataOithona plumifera

Oithona simplex

Oncaea conifera

Parvocalanus elegans

Pseudocyclops sp.

Tortanus barbatusTortanus gracilisAcartia pacfica

Acrocalanus gibber

Calanopia aurivillli

Calanopia ellipticaCalanopia thompsonii

Calocalanus sp.

Candacia bradyi

Canthocalanus pauper

Centropages furcatus

Corycaeus asiaticus

Corycaeus catus

Corycaeus crassiusculus

Corycaeus erythraeus

Farranula concinna

Farranula gibbula

Labidocera acuta

Labidocera kroyeri

Labidocera minuta

Microsetella rosea

Oithona rigida

Paracalanus aculeatus

Parvocalanus crassirostris

Subeucalanus subcrassusTemora discaudata

Temora turbinata

Anawekia sp.

Bestiolina similis

Calanopia australica

Copilia sp.

Corycaeus latus

Corycaeus lubbocki

Corycaeus speciosus

Delius sp.

Metis sp.

Oithona setigera

Oncaea mediterranea

Paracalanus denudatus

Pontellopsis herdmani

Tortanus forcipatus

Cyclopoida

Calanoida

Harpacticoida

Poicilostomatoida

TOTAL: 67 species and 4 species group

CORAL = 56

SEAGRASS = 48

SAND = 45

Lubbockia sp.

Tortanus spp.

Acartia erythraea

Oncaea spp.

Abundance: small fraction an order ofmagnitufe higher than large fraction

Diversity: for both size fractions, similar between sites, but offshore stations more diverse and species rich than inshore stations

Small fraction: high abundance but lowdiversity. Large fraction: low abundancebut high diversity

Large fraction: offshore samples collectedat night more species than other samples

A. SMALL FRACTION (100-335 m)

00.10.20.30.40.50.60.70.80.9

1

00.20.40.60.811.21.41.61.82

Shannon H

’

Pie

lou

J

0

5

10

15

20

25

D1C N1C D2C N2C D1CON1COD2CON2CO D1G N1G D2G N2G D1GON1GOD2GON2GO D1S N1S D2S N2S D1SON1SOD2SON2SO 0

2

4

6

8

10

12

14

Species num

ber

Abu

ndan

ce (

x100

0)

0

0.2

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1.2

0

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1

1.5

2

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D1C N1C D2C N2C N1CO N2CO D1G D2G N2G D1GO N1GOD2GON2GO D1S N1S D2S N2S D1SO N1SO D2SO N2SO 0

5

10

15

20

25

30

Shannon H

’

Pie

lou

J

Species num

ber

Abu

ndan

ce (

x100

)

B. LARGE FRACTION (>335 m)

Shannon diversity, Pielou evenness index, species richness, and total abundance in small (A) and large (B) fractions of samples.

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% C

um

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tive

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an

ce

Species rank

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1 10 100

A1

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% C

um

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an

ce

Species rank

B

K-dominance curves of small (A) and large (B) fractions from samples from the three sampling sites.

Canonical correspondence analysis triplot for small fraction samples from three sampling sites.

-1.0 1.0

-1.0

1.0

Ppa

Pac

Pcr

Pel

Bsi

Apa

Agi

Meta

Pse

CasOat

Odeci

Ona

Opl

Osi

OriCspOnc

Kel

Sap

Csc

Eac

Mno

MgrMet

Salinity

Temperature

DissolvedOxygen

Depth

D1C1

D1C3

N1C1

N1C3D2C1

D2C3

N2C1

N2C3

D1CO1D1CO3

N1CO1

N1CO3

D2CO1

D2CO3

N2CO1

N2CO3

D1G1

D1G3

N1G1

N1G3

D2G1

D2G3

N2G1

N2G3

D1GO1

D1GO3

N1GO3

N1GO3D2GO1

D2GO3

N2GO1

N2GO3

D1S1

D1S3

N1S1

N1S3

D2S1

D2S3

N2S1

N2S3

D1SO1

D1SO3

N1SO1

N1SO3

D2SO1

D2SO3

N2SO1N2SO3

-1.0 1.5

-0.8

0.8

AerApa

AgiAgr

Ana

Bsi

Cau

Cau

Cel

Cth

CalCbr

Cpa Cfu

Cor Del

Lac

Lkr

Lmi

Mau

Pac

Pde

Pcr

Pel

Phe

Pse

Ssu

TdiTtuTba

Tfo

Tgr

Tor

Oat

Ode

Ona

Ooc

Opl

Ori

Ose

Osi

Lub

Csc

Ela

EacMgr

Mno

Mro

Met

Cop

Can

Cas

Cca

CcrCer

Cda

Cla

Clu

Csp

Cors

Fgi

Fco

Kel

Oco

OmeOnc

Salinity

TemperatureDissolvedOxygen

Depth

D1C1

D1C3

N1C1N1C3

D2C1

D2C3

N2C1

N2CO3N2CO1

N2C3

D1G1

D1G3

D2G1

D2G3

N2G1N2G3

D1GO1

D1GO3

N1GO1

N1GO3

D2GO1

D2GO3

N2GO3

D1S1

D1S3

N1S1

N1S3

D2S1

D2S3

N2S1

N2S3

D1SO1

D1SO3

N1SO1

N1SO3

D2SO1D2SO3

N2SO1

N2SO3

N2GO1

N1CO1

N1CO3N1CO3

Canonical correspondence analysis triplot for large fraction samples from three sampling sites.

Group1 Group2 Group3a Group3bSpecies IndValij Species IndValij Species IndValij Species IndValijOncaea spp. 35 Oithona plumifera 11 Corycaeus spp. 39 Metacalanus sp. 62Corycaeus spp. 32 Oithona simplex 10 Oncaea spp. 38 Microsetella norvegica 52Microsetella norvegica 32 Parvocalanus elegans 7 Parvocalanus elegans 36 Euterpina acutifrons 45Oithona attenuata 30 Oithona nana 7 Oithona nana 32 Oithona nana 33Oithona nana 28 Microsetella norvegica 6 Oithona simplex 32 Oithona simplex 31Oithona simplex 28 Acartia pacifica 6 Oithona attenuata 28 Parvocalanus elegans 30Parvocalanus elegans 27 Kelleria sp. 6 Euterpina acutifrons 22 Clytemnestra scuttelata 24Euterpina acutifrons 21 Oithona decipiens 6 Metis sp. 21 Sapphirella-type 22Oithona rigida 21 Pseudocyclops sp. 6 Paracalanus parvus 19 Corycaeus spp. 21Acrocalanus gibber 13 Oncaea spp. 3 Bestiolina similis 16 Oncaea spp. 20Parvocalanus crassirostris 13 Corycaeus spp. 3 Paracalanus aculeatus 13 Oithona rigida 17Sapphirella-type 11 Euterpina acutifrons 2 Oithona rigida 9 Oithona attenuata 11Calanoida spp. 6 Macrosetella gracilis 2 Oithona plumifera 7 Paracalanus parvus 2Macrosetella gracilis 3 Metacalanus sp. 1 Sapphirella-type copep. 5Bestiolina similis 2 Oithona attenuata 1 Macrosetella gracilis 5Metacalanus sp. 1 Sapphirella-type 1 Microsetella norvegica 3Metis sp. 1 Paracalanus parvus 1 Metacalanus sp. 1

17 17 17 13

SEAGRASSinshore (day & night)offshore (day & night)

SANDAll day inshore and offshore

CORALinshore (day & night)offshore (day & night)

SANDAll night inshore and offshore

SEAGRASSinshore (day & night)offshore (day)

SEAGRASSoffshore night

SANDinshore (day & night)offshore (day)

SANDoffshore nightCORAL

inshore (day & night)offshore (day)

CORALoffshore night

Group1a IndValij Group1b IndValij Group2a IndValij Group2b IndValij Group3a IndValij Group3b IndValij

Metis sp. 72 Anawekia sp. 50 Microsetella norvegica 72 Oithona simplex 80 Acrocalanus gibber 23 Metacalanus aurivilli 27

Oncaea spp. 49 Calanopia australica 50 Macrosetella gracilis 47 Microsetella norvegica 62 Paracalanus aculeatus 22 Farranula gibbula 23

Corycaeus lubbocki 38 Centropages orsini 50 Centropages orsini 34 Euterpina acutifrons 51 Temora turbinata 22 Acartia pacfica 22

Corycaeus andrewsi 35 Pontellopsis herdmani 50 Oithona oculata 17 Oncaea conifera 36 Corycaeus asiaticus 17 Oithona rigida 20

Oithona setigera 25 Calanopia elliptica 27 Pseudocyclops sp. 15 Parvocalanus elegans 36 Centropages furcatus 16 Corycaeus erythraeus 18

Bestiolina cf. similis 13 Subeucalanus subcrassus 26 Oncaea spp. 13 Corycaeus andrewsi 35 Temora discaudata 15 Oncaea conifera 17

Copilia sp. 13 Acartia pacfica 19 Parvocalanus crassirostris 13 Oithona plumifera 30 Parvocalanus crassirostris 15 Microsetella rosea 17

Corycaeus latus 13 Labidocera minuta 10 Oithona plumifera 10 Kelleria spp. 29 Oithona rigida 13 Oithona plumifera 15

Corycaeus speciosus 13 Calanopia aurivillli 9 Corycaeus andrewsi 9 Corycaeus spp. 25 Canthocalanus pauper 12 Acrocalanus gibber 14

Delius sp. 13 Calanopia thompsonii 9 Corycaeus asiaticus 7 Oithona nana 23 Acartia erythraea 11 Corycaeus crassiusculus 14

Oncaea mediterranea 13 Oithona plumifera 7 Acrocalanus gracilis 7 Oithona attenuata 21 Metis sp. 10 Paracalanus aculeatus 13

Paracalanus denudatus 13 Corycaeus asiaticus 7 Acartia pacfica 7 Parvocalanus crassirostris 20 Calanopia aurivillli 10 Subeucalanus subcrassus 13

Pseudocyclops sp. 13 Kelleria spp. 7 Euterpina acutifrons 6 Macrosetella gracilis 20 Corycaeus crassiusculus 10 Corycaeus asiaticus 12

Tortanus forcipatus 13 Acrocalanus gibber 7 Oithona nana 4 Acartia pacfica 19 Oncaea conifera 9 Centropages furcatus 10

Calanopia aurivillli 12 Parvocalanus crassirostris 6 Oncaea conifera 4 Acrocalanus gracilis 17 Microsetella rosea 9 Canthocalanus pauper 9

Acartia pacfica 11 Oithona oculata 6 Corycaeus spp. 4 Corycaeus dahli 17 Subeucalanus subcrassus 9 Candacia bradyi 8

Acrocalanus gibber 8 Corycaeus crassiusculus 6 Oithona rigida 4 Tortanus barbatus 17 Corycaeus erythraeus 8 Labidocera acuta 8

Parvocalanus elegans 5 Temora turbinata 6 Microsetella rosea 3 Tortanus spp. 17 Farranula concinna 6 Macrosetella gracilis 7

Parvocalanus crassirostris 5 Microsetella norvegica 5 Oithona simplex 3 Corycaeus asiaticus 17 Euterpina acutifrons 6 Microsetella norvegica 6

Corycaeus catus 5 Centropages furcatus 5 Paracalanus aculeatus 3 Oithona decipiens 13 Calanopia elliptica 4 Euterpina acutifrons 5

Oithona plumifera 4 Parvocalanus elegans 5 Parvocalanus elegans 2 Oithona rigida 9 Acartia pacfica 4 Oithona nana 4

Farranula gibbula 3 Microsetella rosea 4 Acrocalanus gibber 2 Metacalanus aurivilli 8 Labidocera minuta 4 Kerellia spp. 4

Oithona decipiens 3 Temora discaudata 3 Subeucalanus subcrassus 2 Oithona oculata 6 Calocalanus sp. 4 Clytemnestra scutellata 4

Corycaeus erythraeus 3 Macrosetella gracilis 3 Canthocalanus pauper 1 Canthocalanus pauper 4 Lubbockia spp. 4 Calanopia aurivillli 4

Metacalanus aurivilli 3 Farranula gibbula 3 Kelleria spp. 1 Oncaea spp. 4 Corycaeus spp. 3 Corycaeus catus 4

Oithona rigida 2 Metis sp. 2 Clytemnestra scutellata 1 Paracalanus aculeatus 3 Calanopia thompsonii 3 Parvocalanus crassirostris 3

Centropages furcatus 2 Canthocalanus pauper 2 Acartia erythraea 1 Corycaeus erythraeus 3 Corycaeus catus 3 Labidocera minuta 3

Corycaeus spp. 2 Oithona rigida 2 Clytemnestra scutellata 2 Farranula gibbula 3 Temora discaudata 3

Temora turbinata 1 Euterpina acutifrons 1 Acrocalanus gibber 2 Macrosetella gracilis 3 Oithona attenuata 3

Calanopia elliptica 1 Corycaeus erythraeus 1 Subeucalanus subcrassus 1 Oithona oculata 2 Temora turbinata 2

Microsetella norvegica 1 Oncaea conifera 1 Calanopia elliptica 1 Oithona plumifera 2 Farranula concinna 2

Clytemnestra scutellata 1 Corycaeus spp. 1 Acartia erythraea 1 Clytemnestra scutellata 2 Calanopia elliptica 1

Subeucalanus subcrassus 1 Corycaeus andrewsi 1 Corycaeus catus 1 Parvocalanus elegans 1 Oithona simplex 1

Corycaeus crassiusculus 1 Oithona nana 1 Centropages furcatus 1 Microsetella norvegica 1 Metis sp. 1

Labidocera minuta 1 Corycaeus spp. 1

Calanopia aurivillli 1

Temora turbinata 1

34 34 27 37 34 35

SUMMARY1. Identified 65 copepod species from small and large fractions of samples that

make up communities from coral, seagrass and sand substrates

2. On community structure:

a. High species richness and low abundance for large fraction but the reverse for small fraction likely due to dominance effects

b. Overall species diversity similar between sites due to high variability between samples

c. Inshore stations had lower species richness than offshore stations for both size fractions for all sites probably due to biological interactions like predation and competition; highest species richness in offshore stations at night for large fractions likely related

withadvection and diel vertical migration

d. Site and time - specific assemblages or groups were explicitly identified by CCA

e. Site- and time-specific Indicator species and assemblage were clearly defined in large fraction samples

THANK YOU FOR YOUR ATTENTION

Addresses of other authors4Institute of Bioscience, Universiti Putra Malaysia, 43400 UPM, Serdang, Selangor, Malaysia

5Takehara Station, Faculty of Applied Biological Science, Hiroshima University 5-8-1 Minato-machi, Takehara, Hiroshima 725-0024, Japan

6Div. of Zoology, Research Center for Biology – LIPI, Jl. Raya Bogor Km. 46 Cibinong 16911, Indonesia

7Institute of Oceanic Research & Development, Tokai University 3-20-1 Orido, Shimizu, Shizuoka 424-8610 Japan

8Faculty of Bioresources, Mie University, 1515 Kamihama-cho, Tsu 514-8507, Japan

9Department of Environmental Engineering for Symbiosis, Faculty of Engineering, Soka University

10Usa Marine Biological Institute, Kochi University, Usa-cho, Tosa, Kochi 781-1164, Japan

11Graduate School of Environment and Information Sciences, Yokohama National University 79-2 Tokiwadai, Hodogaya, Yokohama 240-8501, Japan

12Department of Marine Biological Resource and Ecology, Institute of Marine Environment and Resources

246 Danang Street, Haiphong City, Vietnam

13Department of Marine Plankton, Institute of Oceanography, Cau Da 01, Vinh Nguyen, Nha Trang, Vietnam

14Institute of Marine Science, Burapha University, Bangsaen, Chonburi, 20131 Thailand

15Division of Biological Sciences, University of the Philippines in the Visayas, Miagao, Iloilo 5023, Philippines