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Reproduction strategies of stony corals (Scleractinia) in an equatorial, Indonesian coral reef [Elektronische Ressource] : contributions for the reef-restoration / vorgelegt von Sascha Bernd Carsten Romatzki

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Reproduction strategies of stony corals (Scleractinia) in an equatorial, Indonesian coral reef. Contributions for the reef-restoration Dissertation zur Erlangung des Doktorgrades der Naturwissenschaften – Dr. rer. nat. – im Fachbereich 2 (Biologie/Chemie) der Universität Bremen vorgelegt von Sascha Bernd Carsten Romatzki angefertigt am Zentrum für Marine Tropenökologie Center for Tropical Marine Ecology Bremen 2008 Gutachter der Dissertation: 1. Gutachter: Prof. Claudio Richter 2. Gutachter: Dr. Andreas Kunzmann Mitglieder der Prüfungskommssion: 1. Prüfer: Prof. Kai Bischof2. Prüfer: Dr. Uwe Krumme 1. weiteres Mitglied: Cornelia Roder2. weiterAnne Buhmann Tag des öffentlichen Kolloquiums: 30. Januar 2009 „So eine Arbeit wird eigentlich nie fertig, man muss sie für fertig erklären, wenn man nach Zeit und Umständen das Möglichste getan hat.“ (Goethe; zur Iphigenie, aus der Italienischen Reise 1786)List of PapersThis thesis is based on the scientific publication listed below. The specific contributions of each of the authors in term of idea and concept development, data aquisition and analysis, as well as manuscript writing for the respective publication are indicated.Publication ITitle: Determination of fine-scale temporal variation in acroporid and pocilloporid settlement in North Sulawesi, IndonesiaAuthors: S.B.C. Romatzki and A.

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Reproduction strategies of stony corals
(Scleractinia) in an equatorial, Indonesian coral reef. Contributions for the reef-
restoration

Dissertation zur Erlangung des Doktorgrades der
Naturwissenschaften
– Dr. rer. nat. –
im Fachbereich 2 (Biologie/Chemie)
der Universität Bremen

vorgelegt von
Sascha Bernd Carsten Romatzki

angefertigt am
Zentrum für Marine Tropenökologie
Center for Tropical Marine Ecology
en 2008emrB

Dissertation: derGutachter

1. Gutachter: 2. Gutachter:

Prof. Claudio Richter

Andreas Kunzmann . Dr

Prüfungskommssion: derMitglieder

1. Prüfer: 2. Prüfer:

Prof. Kai Bischof

. Uwe Krumme Dr

Cornelia Roderes Mitglied: 1. weiter

Anne Buhmannes Mitglied: 2. weiter

fentlichen Kolloquiums: 30. Januar 2009 ag des öfT

d eigentlich nie fertig, Arbeit wir„So eine

man muss sie für fertig erklär en,

wenn man nach Zeit und Umständen das Möglichste getan hat.“

(Goethe; zur Iphigenie, aus der Italienischen Reise 1786)

List of Papers

This thesis is based on the scientific publication listed below

The specific contributions of each .

of the authors in term of idea and concept development, data aquisition and analysis, as well as

manuscript writing for the respective publication are indicated.

Publication I

Determination of fine-scale temporal variation in acroporid and pocilloporid settlement in itle:T

North Sulawesi, Indonesia

A. Kunzmann S.B.C. Romatzki and Authors:

Marine Ecology Progress Series (submitted)Journal:

The original idea and concept of this publication was developed by S.B.C. Romatzki, who also

independently conducted all of the fieldwork and sample processing. Data analyses were carried

The manuscript was written by S.B.C. out by S.B.C. Romatzki with input by S. Schmidt-Roach.

A. Kunzmann.Romatzki, with revesions and improvement by

Publication II

Gametogenesis of four scleractinian corals in the Celebes Seaitle:T

Authors:A. Kunzmann S.B.C. Romatzki and

Journal:1th International Coral Reef Symposium (submitted) Proceedings of the 1

The original idea and concept of this publication was developed by S.B.C. Romatzki, who also

The manuscript was written independently conducted all of the fieldwork and sample processing.

A. Kunzmann.by S.B.C. Romatzki, with revesions and improvement by

Publication III

Acropora transplants: Determining the influence of an electrical field on the performance of itle:T

Comparison of various transplantation structures

S.B.C. RomatzkiAuthor:

Journal of Experimental Marine Biology (submitted)Journal:

The original idea and concept of this publication was developed by S.B.C. Romatzki, who also

independently conducted all of the fieldwork and sample processing. The concept of experiment

3 in this publication was developed by S.B.C. Romatzki, S.C.A. Ferse and E. Borell. Data analy-

The manuscript was written by ses were carried out by S.B.C. Romatzki with input by E. Borell.

S.B.C. Romatzki, with revesions and improvement by M. Schmid, K. von Juterzenka and J.-H.

fen.Stef

Content

Acknowledgements………………………………………………………………….……….....I

Summary…………………………………………………………………………….………..III

Zusammenfassung…………………………………………………………………….……...VI

Thesis Overview……………………………………………………….………....1 1 – Chapter

1. General Intr

1.1.2

1.1.3

oduction…………………………………………………………….……….....3 1.1 Reproduction in scleractinian corals……………………………………….………..3

1.1.1 Asexual ……………………………………………….……..3oductioneprr

……………………………………….…….………...4oductioneprrSexual

…………………………………………………................4spawningMass

oduction in high latitude vs equatorial r1.1.4 Repreefs………………...............5

1.2 Reef restoration and reef rehabilitation……………..…………………….……..….6

……………………………………………………..………6os and cons1.2.1 Pr

estoration” and what is “r1.2.2 What is “rehabilitation” then……….…….….7

………………………………………….……....7oaches1.2.3 Old and new appr

………………………………………….……....91.2.4 Using of coral fragments

Aims of the thesis…………………………………………………………….……..91.3

2. General Material & Methods……………………………………………………….…….10

Area………………………………………………………………....….…...10Study 2.1

iles……………………………………………………………….…...1T2.2 Settlement 1

2.3 In situ monitoring of reproduction status…………………………………….....…12

2.4 Histological preparation for examination of reproduction status……………….....13

2.5 Surface estimation and zooxanthella-count of coral fragments………………..….14

3. General Results & Discussion…………………………………………………………….14

3.1 Reproduction and settlement in equatorial reefs: continuous with seasonal

peaks……………………………………………………………………….…..…14

3.2 Manipulation of coral longitudal growth enhancement……………………….......16

emarks………………………………………………………………….…....174. Concluding r

ences………………………………………………………………………….………195. Refer

I………………………………………………………………………….27 2 – PaperChapter

Determination of fine-scale temporal variation in acroporid and pocilloporid settlement in

North Sulawesi, Indonesia

II………………………………………………………………………...50 3 – PaperChapter

Gametogenesis of four scleractinian corals in the Celebes Sea

III………………………………………………………………………..64 4 – PaperChapter

Determining the influence of an electrical field on the performance of

Comparison of various transplantation structures

transplants: oporaAcr

Appendix……………………………………………………………………………………..92

Disclaimer…………………………………………………………………………………....94

Acknowledgements

f for agreeing to supervise this thesis in first place, but olfWI would like to thank Prof. Matthias

, who took over the supervision in the very last minute special thanks go to Prof. Claudio Richter

Thanks a lot to both for making the change so uncomplicated. I due to a very tide time schedule.

Andreas Kunzmann, who implemented the idea to conduct a PhD . further would like to thank Dr

thesis in Indonesia and encouraged me to step into the unknown, for his guidance and criticism

throughout the thesis.

My deepest gratitude goes to some very special people in Manado for their generous sponsoring

Thanks to ithout their help I never would have been able to conduct this thesis: Wand support.

Christiane Mueller from Froggies Divers who gave me shelter from the first day of my arrival,

who showed me suitable sites for my project, who gave me my first lessons in Manado Culture

get the uncountable tank-fillings and meals. I also would like to thank and lifestyle. Not to for

, their Hanne Darbol and Gaspare Davi from Gangga Resort and Spa for their generous hospitality

always warm and heartfelt welcome, their unlimited support, interest and open minds for new

. project ideas. Staying at your places was always a feeling of coming home with a touch of holiday

f of these wonderful resorts who always were very helpful.Thanks also to all the great staf

Special thanks to Sebastian Ferse, my roommate, dive buddy and colleague, who was often the

only source of inspiration and scientific input. Despite many difficulties during all the time we

t have been able to conduct my project in Manado without , I for sure wouldn’spend together

him.

Sebastian Schmidt – our MSc student, who came at the “right” time – I would like to thank a

lot for many delicious pancakes…well and some other things of course – but they were not that

Thanks also to Leyla Knittweis and in particular Esther Borell, for collective important ;)….

fering and many encouraging phone calls.suf

Further thanks are dedicated to Fontje Kaligis and family for taking care of me during the first

ambajong Tganized in Manado. Prof. Eddy weeks of my arrival and their help in getting my life or

. for his generous lessons in histological technique and for letting me use his private laboratory

for their assistance with coral tissue preparation and histological Tere and Mer from UNSRAT

sectioning.

Thanks also to those people, who helped me at one point or another in Manado: Dr

. Ineke

Rumengan, who helped me with organizational issues at UNSRAT-University, Asci and Francesco

Angelique & Paul from Murex and Jaakko from Living for a relaxing time on their liverboard,

Colours for help in dive logistics as also Jan & Henriette Bebe for their European humor and

Danish “friendliness”.

I

otok Histirianato for excellent work and help TFollowing people from IPB I would like to thank:

Aktani for supervision, Neviaty Zamani and Pak isa, Unggul Vwith the

and use of the microscope camera.

ganization Adi for the or

I further would like to thank the German community in Indonesia, starting with Harry Palm

s scientific advice, Karen von Juterzenka & Michael and family for their hospitality and Harry’

ganization of a microscope, Schmidt for several weeks of accommodation, supporting words, the or

fen for being a port in numerous corrections on the papers and their friendship, Jan-Henning Stef

stormy seas and a second home during times in Jakarta, Landry Pramoedji and Lutz Kleeberg for

letting me stay in their house for such a long time during the final steps of this thesis.

I also would like to thank Eberhard Krain for being the knight in shining armor when help was

most needed.

Andrew Baird, Sangeeta Mangubhai and Nami Okubo gave many helpful comments, corrections

and clarified questions regarding coral recruitment and histology

answers and provision of your papers.

Thanks for your very prompt .

This study was supported by a PhD scholarship of the DAAD (German

Service). I especially would like to thank Frau Krüger

support during the time of the scholorship.

Academic Exchange

-Rechmann and Brigitte Gerlach for their

My Carol I would like to thank for accompanying me during bad and better times and many

. culinary experiences making the work on this thesis a whole lot easier

And last but not least my dear parents Helga & Paul Romatzki who gave me all the support on

rotz der vielen freundlichen Hilfe und Unterstützung, die ich von dritter Tearth to fulfill my dream.

Seite erfahren habe, wart letztendlich Ihr es, die diese

Anfang bis Ende ermöglicht Arbeit von

habt. Danke für Euren nie endenden Zuspruch, Eure Geduld und Eure Unterstützung.

II

Summary

In the present dissertation the sexual and asexual reproduction-strategies of stony corals in an

equatorial Indonesian coral reef will be examined. Special attention is applied to the seasonality

of sexual reproduction through coral larvae in an important, but yet by coral literature disregarded

Ageographical region, the so-called “coral triangle”. crucial criterion for countries to be accepted

This high as members were coral reef regions with a coral diversity of more than 500 species.

diversity is unique worldwide and is not even surpassed by the world famous Great Barrier Reef

The outlines of this triangle are marked by the Philippines s circa 360 species of stony corals. and it’

est Guinea and Papua New Guinea in the Win the North, Malaysia and Indonesia in the South and

East. Sulawesi, as one of the three biggest main islands of Indonesia, is located in the middle of

The present work examined reefs in and around the Bunaken National Park in North the triangle.

Sulawesi in the Celebes Sea.

The research area was chosen, as there is only few or almost no existing literature covering the

Asian equatorial reefs – especially in Indonesia. reproduction timing and cycles of south-east

Furthermore the here examined reefs are still in good condition as the implementation of the

Bunaken National Park in 1991 lead to a strong decrease of dynamite fishing compared to other

Also the industrialization in this region is not parts of Indonesia where it is still very common.

as progressive as to be noticeably negative for the surrounding reefs. wo estuaries mainly cause T

anthropogenic disturbances as they are transporting garbage and wastewater from the seaside

The examined reefs were located outside the influencing factors due to located town of Manado.

the course of the current.

The first chapter of this work deals with the explanation of terms that are often used in context

The with the present topic. Generative sexual and vegetative asexual reproduction are specified.

asexual reproduction through the so-called “budding” plays an important role in growth and

regeneration of corals and coral fragments. Coral fragments on the other hand have an important

ferences between reef restoration The diffunction in reef restoration and rehabilitation projects.

and rehabilitation will be examined closer as both terms are often used in the wrong context.

ferentiate from each other as the former aims for the Both are manipulating interventions that dif

previous natural condition while latter often uses elements and structures that are not equivalent

to the natural condition.

The second chapter deals with the settlement of coral larvae on artificial settlement tiles in a

. quantitative studyThree settlement frames were permanently installed in each of four reef sites

. Each frame contained 12 tiles at a depth of 5 m with a distance of 25 to 50 m between each other

The examination of the bleached tiles showed, that that were replaced at two-month intervals.

Acroporidae and Pocilloporidae. So-called growth charts were the primary settlers were larvae of

Acroporidae and Pocilloporidae recruits with weekly used to determine the time of settlement of

. accuracyAlthough larvae of both families were found year round, those of the

Acroporidae

III

An intensified increase in acroporid recruits could be noticed showed clear seasonal patterns.

April weeks of 2006 and 2007 as also between May and June 2006 and 2007.during the

Settlement plates were able to give information about the peak reproduction times of coral families

but not of single species, as current techniques of coral recruit identification for this application

are not reliable enough.

Chapter 3 tried to close this information gap by focusing on the reproduction strategy and cycles of

These species were chosen four selected coral species by histological examination of their tissues.

after a visual assessment of the examined reef sites in terms of their abundance and the possibility

Therefore all chosen species were those with a branching growth for easy and multiple sampling.

form. Whereas Seriatopora hystrix is a brooder, Pocillopora verrucosa, Acropora yongei and

The coeval presence of planula-larvae, ovaries and are known to be spawners. opora pulchra Acr

-specimens from difS. hystrixspermaries in all -around ferent sampling times referred to a year

brooding in the examined sites. Ripe eggs, which are spawned together with spermaries as reddish

A. pulchra in June 2006 and May 2007 and in A. yongeiegg-sperm-bundles, could only be found in

The presence April/May 2006 and March 2007 - suggesting a single annual reproduction cycle. in

is a indicator for a imminent spawning, as zooxanthellae appear verrucosa.Pof zooxanthellae in

three to four days before this event in eggs of this species. Zooxanthellae were found in eggs in

August suggesting there is a biannual gametogenic January and March, as also between July and

cycle for this species in North Sulawesi.

The fourth and last chapter deals with the hypothesis of enhanced growth of coral fragments

transplanted in and exposed to an electrical field. The hereby examined technique is based on the

ged in saltwater electrolysis that uses a low current between an anode and a cathode both submer

The cathode is used as an artificial reef structure. Due to a higher Ion-concentration at . saltwater

the cathode, precipitation takes place on its surface in the form of lime scale analog to natural

. ith accelerating coating the structure gains size and stabilityWlimes stone as found in the reef. The

The unlimited rough surface of the accretion is a suitable settlement substrate for marine larvae.

possibilities in cathode design allow a wide range for an application in reef rehabilitation. So far

the observed enhancement of coral growth by the inventors remains in question and has lead to

controversy among scientists as only very few studies have been published in regards to this topic.

Common consensus is that enhanced coral growth is due to the enhanced Ion-concentration and the

resulting increase of the pH-value in approximate distance to the cathode. Finger sized fragments

of A. yongei and A. pulchra were transplanted on three different constructions for the clearance

ferent aspects. In the first experiment two tunnel shaped structures were connected to two of dif

fect on the growth of corals. In a ferent electrical currents to test if intensity of current has an efdif

ferent heights. second experiment fragments were transplanted to table-like structures each with dif

Here differences in growth performance were tested to find the ideal transplantation elevation. In

a third experiment fragments transplanted in direct contact to the cathode material were compared

to those only transplanted within an electrical field and without direct cathode contact. Controls

IV

with similar designs to the cathodes but without electricity were used for all three experiments.

Furthermore growth rates of branches within the donor colonies were measured. Results of all

experiments showed no unusual increased growth for the used transplants.

with “uncharged” controls showed no or negative significant growth dif

direct comparison A

comparison Aferences.

of growth data from the transplants and remaining branches from the donor colonies showed

significant lower growth rates for the transplants. Best results were achieved with the lowest

mA (approximately 1.67 Acurrent of 7

-2) and when fragments were exposed to the electrical

mAfield but not in direct contact to the cathode or exceeding 1.67

ferently between experiments.transplants performed dif

-2The results also showed that .

These results differ significantly from the observations of the developers, who claimed five to

twenty times higher coral growth on electrical structures. Insights gained from these experiments

will help to facilitate the planning of future rehabilitations projects when making decisions on

transplant species, size, cathode design and operational current.

V

Zusammenfassung

In der vorliegenden Dissertation werden die sexuellen als auch die asexuellen

von ausgewählten Steinkorallen in einem äquatornahen, indonesischem Reproduktionsstrategien

ermehrung VAufmerksamkeit galt der Saisonalität der sexuellen f untersucht. Besondere Korallenrif

durch Korallenlarven in einer wichtigen, aber bisher in der Korallenliteratur vernachlässigten

Als ausschlaggebendes Kriterium für geographischen Region, dem so genannten Korallendreieck.

Aufnahme von ausgewählten Gebieten der Mitgliedsstaaten galt eine Korallenvielfalt von mehr die

als 500 Artenvielfalt ist weltweit einzigartig und kann auch von dem weltbekannten Arten. Diese

Great Barrier Reef mit seinen circa 360 Steinkorallenarten nicht überboten werden. Die heutigen

esten und Papua WMitgliedstaaten der Philippinen im Norden, Malaysia und Indonesien im

Neuguinea im Osten bezeichnen die Grenzen des Dreiecks. Sulawesi als eine der drei großen

Hauptinseln Indonesiens, befindet sich in der Mitte dieses Dreiecks. Die in der vorliegenden

fe liegen im und um den Bunaken Nationalpark im Norden Sulawesis in Arbeit untersuchten Rif

der Celebes See.

Das Untersuchungsgebiet wurde auf Grund der wenigen bzw

. kaum existierenden

Veröffentlichungen bezüglich der Vermehrungszeiten und –zyklen von äquroerialen Korallen - im

fen - gewählt. Des Besonderen in indonesischen Riffe in einem guten eiteren befinden sich die RifW

Zustand da vor allem durch die Implementation des Nationalparks 1991 das Dynamitfischen im

Auch ist die Industrialisierung fen stark zurückgegangen ist. erhältnis zu anderen indonesischen RifV

in dieser Region noch nicht soweit fortgeschritten, als das diese sich merkbar negativ auf die

fe auswirken. umliegenden Riffmündungen Anthropologe Störungen sind vor allem auf zwei Rif

fe und erhöhte Mülleinträge der anliegenden Stadt Manado zurückzuführen. Die untersuchten Rif

lagen auf Grund des Strömungsverlaufs außerhalb dieser Einflussfaktoren.

fen, die häufig in Arbeit beschäftigt sich mit der Erklärung von BegrifDas erste Kapitel dieser

Thematik genannt werden. Es wird auf die generative sexuelle erbindung mit der vorliegenden V

ermehrung durch Vermehrung eingegangen. Die asexuelle Vals auch auf die vegetative asexuelle

achstum und der Regenerierung Wdas so genannte “budding” spielt eine wesentliche Rolle im

von Korallen und Korallenfragmenten. Korallenfragmente wiederum spielen eine große Rolle bei

frestaurierungs und –rehabilitierungsmaßnahmen. Die Unterschiede zwischen RifRiffrestaurierung

erwechslung näher erläutert. Beide sind Vfrehabilitierung werden auf Grund häufiger und Rif

fe, die sich vor allem darin unterscheiden, dass ersteres eine Rückführung manipulierende Eingrif

des alten Zustands anstrebt, während letzteres sich Elemente und Strukturen bedient, die nicht

dem alten, natürlichen Zustand entsprechen.

Ansiedeln von Korallenlarven auf ausgebrachten Kalksteinplatten Im zweiten Kapitel wird das

Abstand von 25 quantitative untersucht. Hierzu wurden jeweils drei Besiedlungsrahmen in einem

iefe von 5 m in vier verschiedenen Stationen installiert. Jeder Rahmen Tbis 50 Metern und einer

fasste 12 Platten die in 2-monatigen Intervallen gegen neue ersetzt wurden. Die Untersuchung

VI

Acroporidae und Pocilloporidae sich der gebleichten Platten zeigte, dass vor allem Larven von

ansiedelten. Mit Hilfe von Ansiedlungszeit achstumsschlüsseln für diese Familien, konnte die W

oche genau berechnet werden. Obwohl zwar Larven beiden Wder untersuchten Rekruten auf eine

Acroporidae eindeutig saisonelle Peaks. Familien sich ganzjährig ansiedelten, zeigten diese der

Acropora- Rekruten kam es jeweils in den Auftreten von Zu einem verstärkten ochen April-W

2006 und 2007 sowie zwischen Mai und Juni 2006 und 2007.

Da die sichere Bestimmung von Korallenrekruten auf Spezies-Level auf Grund der geringen Größe

Angaben auf Grundlage von issensstand unmöglich ist, konnten keine konkreten Wzum jetzigen

fen werden. Histologische Arten getrofBesiedlungsplatten bezüglich der Laichzeiten für einzelne

Untersuchung im dritten Kapitel zeigen daher an Hand von vier ausgewählten Steinkorallen

Arten wurden Auswahl der deren Fortpflanzungsstrategie und Entwicklungszylen. Bei der

fe am häufigsten in den solche gewählt, die nach visueller Einschätzung der untersuchten Rif

untersuchten Gebieten gefunden werden konnten und eine einfache, multiple Probenentnahme

erlaubten. Alle Arten gehören daher zu den Astbildenden, wobei Seriatopora hystrix als Brüter

sowie Pocillopora verrucosa, Acropora yongei und Acropora pulchra als Laicher bestätigt werden

S. Anwesenheit von Planulalarven, Ovarien und Spermarien in allen konnten. Die gleichzeitige

ermehrung in dem untersuchten Gebiet hin. V-Präparaten weisen auf eine kontinuierliche hystrix

, die zusammen mit Spermien als rote Ei-Sperma-Bündel gelaicht werden, wurden in Reife Eier

Acropora yongei in den Monaten Juni 2006 und Mai 2007 und in A. pulchra im April/Mai 2006

Anwesenheit Ablaichen im Jahr hinweist. Die und März 2007 gefunden, was auf ein einmaliges

von Zooxanthellen in P. verrucosa-Eier sind Anzeichen für ein kurzbevorstehendes Ablaichen, da

age vor dem Ereignis in den Eiern auftauchen. Zooxanthellen wurden TZooxanthellen etwa 3 bis 4

August in Eiern gefunden, was einen zwischen Januar und März, als auch zwischen Juli und

Art in Nord Sulawesi wahrscheinlich macht. zweimaligen Gametenzyklus pro Jahr in dieser

Das vierte und letzte Kapitel befasst sich mit der Hypothese, dass Korallentransplantate,

achstum aufweisen. Die hierbei Wdie einem elektrischen Feld ausgesetzt sind ein erhöhtes

Anlegen einer -Elektrolyse, bei der es bei echnik basiert auf der SalzwasserTuntersuchte

Anode und Kathode zu Kalkfällung durch erhöhte Ionen-niedrigen Spannung zwischen einer

Konzentrationen an letzterer kommt. Die Kathode wird hierbei als künstliches Riff-Substrat

benutzt. Der mit der Zeit wachsende Kalkmantel entspricht in der Zusammensetzung dem vom

, mit einer achsen der eigentlichen KathodenstrukturWnatürlichen Korallenkalk und führt zu einem

fenheit dieses Kalkmantels macht ihn zu einem gehenden Stabilitätszunahme. Die Beschafeinher

ganismen. Den gestalterischen Möglichkeiten idealen Siedlungssubstrat für Larven mariner Or

frehabilitierung keine Grenzen gesetzt. Anwendung in der Rifder Kathodenstruktur sind in der

achstums von Korallen, die Wfekt eines erhöhten Der von den Erfindern beobachtete Nebenef

auf diesen Strukturen wachsen wurde bisher kaum wissenschaftlich untersucht und führte zu

kontroversen Diskussionen unter Wissenschaftlern. Von einigen Autoren wird die erhöhte Ionen-

ert in Kathoden-Nähe als mögliche Ursache für Konzentration und dem daraus erhöhten pH-W

VII

achstum betrachtet. Fingerlange Fragmente der beiden Werhöhtes

Acr A. yongei-Arten opora

wurden auf drei verschiedenen Konstruktionen zur Klärung unterschiedlicher A. pulchraund

Aspekte transplantiert. In einem ersten Experiment wurden zwei tunnelartige Strukturen mit

unterschiedlichen elektrischen Spannungen betrieben, um festzustellen ob Unterschiede einen

fekt haben. In einem zweiten Experiment wurden die in Längenwachstum nachweisbaren Ef

Fragmente auf tischartige Gestelle transplantiert, die sich in der Höhe unterschieden. Hierbei

ransplantations-Höhe gibt, die sich in Unterschieden Tsollte untersucht werden, ob es eine ideale

achstum bemerkbar macht. In einem dritten Experiment wurde der Unterschied zwischen Wim

Fragmenten, die in direktem Kontakt mit der Kathode stehen und solchen die sich lediglich in

einem elektrischen Feld ohne direkten Kontakt zur Kathode stehen, untersucht. Für alle drei

Außerdem Experimente gab es Kontrollstrukturen in jeweils gleichem Design jedoch ohne Strom.

achstumsraten von “normalen” Zweigen innerhalb der Spenderkolonien gemessen. Wwurden

achstum für die Wgebnisse zeigten in den verschiedenen Experimenten kein erhöhtes Alle Er

verwendeten Transplantate: Ein direkter Vergleich mit den “ungeladenen” Kontroll-Strukturen

zeigte keine bis negative signifikante Wachstumsunterschiede. Ein Vergleich der Wachstumsraten

mit denen von verbleibenden Ästen in den Spenderkolonien zeigte hingegen signifikant niedrigere

(ca. Agebnisse wurden unter geringster Spannung von 7 achstumsunterschiede. Beste ErW

1.67 A m-2), bzw. in einem elektrischen Feld erzielt, jedoch nicht bei einem direkten Kontakt

mAmit der Kathode oder einer Spannung über 1.67

-2gebnisse auch Allerdings zeigten die Er.

unterschiedliche Performance zwischen den einzelnen Experimenten.

Diese Er, die allgemein gebnisse unterscheiden sich erheblich von den Beobachtungen der Erfinder

von einem fünf bis zwanzigfach erhöhtem Korallenwachstum sprechen. Erkenntnisse aus diesen

drei Experimenten sollen dabei helfen, die Planung zukünftiger Projekte, und die

Korallenarten, Größe, Kathoden-Design und Stromstärke zu erleichtern.

ahl der W

VIII

1 Chapter

Thesis Overview

1

2

1. General

1.1

Introduction

oduction in scleractinian coralsRepr

Reproduction is the biological process that leads to the production of new or

ganisms. It is a

ganism is the result of reproduction. Reproduction fundamental feature of all known life as every or

The term “sexual” can also be referred to as can be divided into two types: sexual or asexual.

generative, while the term “asexual” as vegetative. The distinction between sexual and asexual

reproduction is biologically insignificant in the phylum Cnidaria (order Scleractinia), as borders

between these reproduction types are blurred: Cnidarians often can reproduce in both ways and

show a great variety in either of the two (reviewed in Fautin 2002).

oductioneprr1.1.1 Asexual

, due to the high plasticity of their tissue, a wide variation in asexual reproduction Corals display

modes (Harrison and Asexual propagules can be produced e.g. via polyp bailout allace 1990). W

(Sammarco 1982), development of anthocauli (Krupp et al. 1993), asexually produced planulae

The latter is a main feature in the aylor 1969). Tyre and Resing 1986), or budding (Rosen and (A

, when a parent polyp divides itself in order Scleractinia and takes place either intratentacularly

, when daughter polyps form on the side of the two or more daughter polyps, or extratentacularly

The manner by which it reproduces eron 2000). parent polyp. Sometimes, both forms are found (V

The interconnection of the polyps with each other is a significant . influences the shape of the colony

Acroporidae, the term “coral part of life history in colonial corals. In branching corals such as most

growth” most often refers to “longitudal length increase”. This should not be confused with linear

skeletal extension of individual axial polyps through enhanced calcification in the apical region

of the branch (Goreau and Goreau 1959, Oliver 1984), as it rather is the increase in branch length

Thus, the through asexual reproduction of polyps and the growth of their associated skeleton.

axial polyp is the parent polyp that does both - growing in length and budding extratentacularly

Although the term “reproduction” is generally only used when ainwright 1963, Gladfelter 1983). (W

gametes are involved (e.g. Fadlallah 1985, Sier and Olive 1994), it is important to understand that

most “coral growth”-literature does indeed describe the consequences of asexual reproduction, as

it is not strictly referring to the extension of single polyps, but rather to the extension of colony

.dimensions caused by the increase in polyp number within a colony

Further forms of asexual reproduction are to be found in the partial displacement or fragmentation

of coral colonies caused by natural physical impacts of heavy waves and moving objects (Highsmith

These fragments have the ability to survive, reattach to a suitable substratum and establish 1982).

new fecund clone colonies, so that the whole process contributes to the distribution of the species

3

and is seen as a further reproduction strategy. Both restoration and rehabilitation projects often

take advantage of this evolutionary adaptation by employing transplantation of coral fragments as

a tool, as will be discussed in later chapters.

oductioneprr1.1.2 Sexual

The individual polyps of colonial or solitary corals can be further divided into hermaphrodite

or gonochoric animals, which sexually reproduce either as broadcast spawners or brooders.

Porites While most coral species are hermaphrodites, gonochrorism - as found in is Fungia - and

eron 2000). In spawning corals, male and female gametes are released more of an exception (V

simultaneously into the water column, where fertilization and further larval development takes

place. In brooders, on the other hand, fertilization of eggs and growth of planula larvae takes place

inside the polyps, and larvae are released when fully developed and ready to settle.

Early coral reproduction literature saw the brooding mode as the most typical form of sexual

Wreproduction in scleractinian corals (see review by Harrison and allace 1990), while nowadays

- with increasing studies from diverse geographic regions - data reveal that many species are

, both modes are stable within a genus, species spawners (see review by Guest et al. 2005a). Generally

Acroporidae provide one example of , though there are reported exceptions. population or colony

opora Acrferent reproductive behaviour within one genus: while members of the subgenus difare

spawners, species of the subgenus Isopora are brooders (e.g. Acropora brueggemanni, A. palifera).

In Western Australia some colonies of Pocillopora damicornis were reproducing as brooders,

ard 1995). Exceptions within a species while others in the same reef released eggs and sperm (W

, which was reported Pocillopora verrucosafrom geographically divided areas were reported for

as a brooder for one part of the world (Stimson 1978), while in several others it was identified

as a spawner (Fadlallah 1985, Sier and Olive 1994, Kruger and Schleyer 1998). However, as the

is found in an earlier publication, some authors acknowledge the verrucosa .Pbrooding report for

possibility of species misidentification as having lead to wrong conclusions.

spawning1.1.3 Mass

The best-known but not yet completely understood phenomenon of annual cnidarian reproduction

is the “mass spawning” first described from the Great Barrier Reef in Australia. Here, populations

of widespread and abundant corals are spawning together on the same few lunar nights in October

illis et al. 1985, Babcock et al. 1986).Wof each year (Harrison et al. 1984,

Since these early reports from the 1980s, additional observations followed from a wide geographical

range of locations around the world (see Dai et al. 1992, Guest et al. 2002, Bastidas et al. 2005,

, the term “mass spawning” is often used in a context ize et al. 2005). HoweverVHatta 2005,

ferent from the original definition: First described as a “synchronous mass spawning” that dif

involved 105 scleractinian corals resulting into extensive egg-sperm-slicks drifting at the surface,

“mass spawning” nowadays is also used to describe the synchronous gamete release of only few

4

ize Vcoral species or just multiple colonies at the same time (see Bastidas et al. 2005, Hatta 2005,

The term mass spawning also appears in coral reproduction reports from the north et al. 2005).

omascik et al. 1997), without any further reports following. Tcoast of Java in Indonesia (see in

eefsoduction in high latitude vs equatorial rRepr1.1.4

ariations in environmental parameters are commonly believed to influence the onset and timing of V

ferent scale, such as water temperature reproduction in corals. Each of these cues is acting on a dif

and solar insulation for the month or season (Shlesinger and Loya 1985, Penland et al. 2004), tidal

owards Tamplitude for the day of the month and light for the time of night (Harrison et al. 1984).

the equator such parameters have a much narrower range than they have in high-latitude regions.

The previously described mass spawning phenomenon of the Great Barrier Reef is seen to be

directly linked to such fluctuations: Oliver et al. (1988) recorded the geographic extent of mass

spawning from the subtropical (23.5°S) to the tropical Great Barrier Reef (9.5°S).

Their further

comparison of reproduction seasonality and synchrony among and within coral species, distributed

from the southern Great Barrier Reef towards the low latitudes of Papua New Guinea, revealed

a decrease in both, with no occurrence of any great extent in equatorial regions. It is therefore

hypothesized that the breakdown of seasonal and synchronous coral reproduction in low-latitude

New Guinea is the result of the low variability of environmental parameters. Further evidence for

this hypothesis is seen in the absence of mass spawning events in the northern Red Sea, where

environmental parameters are also relatively constant (Shlesinger and Loya 1985).

, mass spawning of corals has been observed in other regions with narrow environmental However

fluctuations such as the low-latitude Solomon Islands (Baird et al. 2001), and in an equatorial

Although Guest et al. (2005b) agree that such fluctuations, reef in Singapore (Guest et al. 2002).

while less varied, are still sufficient for the physiological processes involved in synchronised

gue that mass spawning is more the result of a strong selective pressure spawning, they also ar

promoting reproduction success through synchronisation, than it is the result of the presence of

ferent species of corals need similar As even difstrong fluctuations of environmental parameters.

environmental conditions for a successful reproduction, synchronous reproduction is as likely to

gued that occur in equatorial assemblages as it is at higher latitudes. Guest et al. (2005b) further ar

no coastal environment is truly aseasonal, and therefore reproductive seasonality and some degree

of multispecific spawning may occur even on equatorial reefs.

Although the extended seasonal

patterns of spawning recorded in equatorial Kenya (Mangubhai and Harrison 2008) could support

this statement, the highly asynchronous reproductive patterns of broadcast-spawning corals

in these reefs do not agree with the assertion of Guest et al. (2005b) that mass spawning is a

characteristic of equatorial reefs.

ith only little detailed research and the sometimes contradictory findings for equatorial regions, W

compared to the many detailed reproduction studies from high-latitude reefs, it remains impossible

to determine which of the previous study reflects a general latitudinal trend. More studies on

5

reproduction patterns from a wider range of equatorial regions are needed in order to help elucidate

the extent of synchrony and seasonality in coral reproduction.

1.2

ehabilitationeef restoration and rReef r

s coral reefs declining at a dramatic speed (Precht and Dodge 2002, ith the world’W

Wilkinson

going a remarkable 2004), the disciplines of conservation biology and restoration ecology are under

oung 2000). Beside the conventional passive measures of protecting, managing and growth (Y

conserving marine habitats, active interventions such as the restoration or rehabilitation of coral

reefs are becoming more popular (Clark and Edwards 1995, Jaap 2000, Schuhmacher et al. 2000,

eemin et al. 2006).YFox and Pet 2001, Nonaka et al. 2003,

1.2.1 Pros and cons

forts are controversial topics that are extensively discussed. Reef restoration and rehabilitation ef

Considering the ability of coral reefs to naturally recover from disturbances, a careful consideration

of all pros and cons of such manipulative human interventions is needed.

The success of restoration and the time needed for total reef recover depends on the survival of

coral fragments, as well as the settlement of coral larvae (e.g. Baird and Hughes 1997, Bowden-

successfully settle, coral larvae need a suitable substrate. oTKerby 2003). Where reefs or reef

areas are insufficiently supplied with new recruits due to a lack of suitable settlement substrate,

this self-recovery fails. Examples where self-recovery was found to be unlikely to impossible

are reefs damaged by blast or dynamite fishing, reef flat dredging or coral harvesting – activities

resulting in highly unstable rubble fields (Lindahl 1998, Fox et al. 1999, Fox et al. 2003). In such

fective cases, human intervention in the form of active restoration and rehabilitation can be an ef

measure (Bowden-Kerby 2003).

Modern approaches as proposed by van

reeck and Schuhmacher (1998) are combining T

the authors, oTconservation and rehabilitation measures with their ideas of underwater parks.

Aggregation Device) have two advantages: a) the rehabilitation of one area so-called DAD (Diver

through the deployment of artificial DADs, resulting in “natural” reefs, and b) the conservation of

other areas as a result of the release from pressure caused by extensive dive tourism.

ferent ecological approaches, they forts have difAlthough reef restoration and rehabilitation ef

They are always labor intensive and often cost intensive (Fox et al. have two things in common:

2005). Furthermore, they are always small-scale projects, causing critics to question the high costs

6for the comparably small benefits produced. For example, in Indonesia alone, there are 7.5 * 10

7ha (Spalding and Grenfell 1997), , there are 2.55 * 10ha of coral reefs (Cesar 1996). Globally

gest reef rehabilitation project to date with 7.1 ha in Costa Rica which is in stark contrast to the lar

(Guzman 1991; reviewed in Edwards and Clark 1998).

6

1000 The calculated costs per square meter when using coral transplantation range from $1200 - $1

m-2 in the USA (Rinkevich 2005) to $50 - $73 US m-2 for transplantation in Thailand (Yeemin et

al. 2006).

Beside the economic disadvantages, other authors also see unpredictable ecological consequences:

Restoration or rehabilitation methods involving species manipulation and/or coral transplantation

, fast growing alien coral can influence the basic ecology of a partially intact reef system. Further

species can out-compete local slow growing corals (Bowden-Kerby 2003). Most often these

fast growing species are branching corals that almost directly increase the fish abundance (Ferse

, their fragile structure can also lead to an increase in rubble production when 2008). However

damaged, thus resulting in further destabilization of the surrounding substrate. Nonetheless, as

reef restoration methods have already been established in many areas, it is noteworthy that the

methods used maximize success in fulfilling their – economic – goals (Spieler et al. 2001).

1.2.2

estoration” and what is “rWhat is “rehabilitation” then?The terms “conservation”, “restoration” and “rehabilitation” often lead to confusion and

Therefore the following explanation misunderstanding and are often used in the wrong context.

should give a short overview for better understanding:

. “Conservation” is defined as the preservation and protection of natural habitat and biodiversity

Area) is one of these measures in which (Marine Protected AThe establishment e.g. of an MP

a management of the resources by limiting human activities takes place, rather than a direct

intervention and manipulation of a habitat.

“Restoration” is a human intervention to accelerate the recovery of a natural habitat, or to bring

ap 2000). It is often seen back ecosystems as closely as possible to their pre-disturbance states (Y

forts.as a manipulative tool of conservation ef

“Rehabilitation” on the other hand is the act of partial or full replacement or substitution of

alternative qualities of structural or functional characteristic of an ecosystem (Edwards 1998).

s “reef restoration projects” are using artificial reef elements and would thus, Most of today’

according to the previous definition, constitute “rehabilitation” efforts rather than conservation or

restoration of a habitat.

oaches1.2.3 Old and new appr

In the past, materials such as bottles, Pedi cabs (e.g. Indonesia), ships (e.g. USA) and car tires (e.g.

altemath and Wforts (reviewed in Philippines) were immersed as artificial reefs for restoration ef

These materials turned out to be unsuitable in many cases due Schirm 1995, Pickering et al. 1998).

to their instability and leaching of toxic substances and, in some cases, very limited settlement of

ganisms. In many cases the dumping of such materials was nothing more than an marine sessile or

endeavor to justify the dumping of industrial waste in coastal areas.

Nowadays there are three major “techniques” dominating the attention of the media and public

7

that find application in many rehabilitation projects:

“Reefballs” (Barber and Barber 1994) are spherical concrete structures of approximately 1m

3

ith their hollow structure Wvolume made out of a pH-neutral, environment friendly cement mix.

ganisms. Coral fragments can be attached and diverse holes they can provide shelter for marine or

by underwater epoxy and the rough surface of the spheres provides a suitable settlement substrate

The main disadvantages are the high weight and the number of ganisms. for the larvae of sessile or

units one would need to rehabilitate bigger areas.

“Ecoreefs” are snowflake-shaped porcelain units 0.5 m in diameter with the main aim of providing

a maximum surface area for coral settlement and of stabilizing rubble. Unfortunately the main

components have to be shipped from the place of production to the area where they will be used.

When the components are assembled, transplants are easy to attach on the numerous arms with

cable ties (Razak 2006).

While the previous conventional approaches aimed at the provision of a suitable transplant basis

and the stabilization of substrate without further manipulation, the “mineral accretion technology”

claims to have both a suitable substrate and an active support of transplant performance on a

This approach utilizes the principle of seawater technical basis (Hilbertz and Goreau 1996).

Aelectrolyses to build up a calcium carbonate-coating around the core material. metal structure

itanium mesh Tged in seawater works as a cathode and is the actual substrate basis, while a submer

When a direct current (DC) is established between the deposited close-by functions as the anode.

and magnesium hydroxide [Mg(OH)two electrodes, CaCO] will be deposited on the cathode 23

(Hilbertz 1992). Depending on the induced current, the ratio between the crystalline form of

(Brucite) is shifted. Less current tends to result in the more stable (Aragonite) and Mg(OH)CaCO2 3

This substrate is similar to natural reef limestone in chemical and Aragonite (Hilbertz 1992). form

physical appearance (van The possibilities in cathode design are reeck and Schuhmacher 1997). T

limitless. Its shape and form can be customized for special needs, as long as the material used is

t need more than a common dive The transportation of core structures normally doesn’conductive.

, the use of cable can be extensive if the power source is located on land. operator boat. However

, better power supply solutions (e.g. sea-based solar panels) On the other hand, the use of other

is even more technical and cost intensive. Furthermore the maintenance of cables, connections

and power supply can be intensive. Previous observations indicated that corals transplanted to

The generated these so-called “BioRocks” are growing faster than their natural mother colonies.

enriched water that fect by providing CaCOelectric field is believed to cause this positive side ef3

enhances natural calcification in corals, and by providing extra electrons from the electrochemical

Aprocesses for production, thereby enhancing metabolic efficiency in terms of coral growth PT

-reviewed article has been , only one peerand fecundity (Hilbertz and Goreau 1996). Until today

published in which the authors were able to measure a significant increase in girth growth of the

Y(Sabater and Porites cylindrica transplanted corals, nubbins of ap 2002).

8

1.2.4 Using coral fragments

, When using coral transplants, the primary aim is to gain an immediate increase in coral cover

diversity (Edwards and Clark 1998), and fish abundance (Clark and Edwards 1999). Furthermore

the presence of coral fragments is believed to attract coral larvae, and with that accelerate the

natural colonization by corals (Gittings et al. 1988).

Coral transplantation was used as a restoration tool for the first time in the early 1970s (Maragos

1974). Since then, coral transplantation has found a wide range of applications in restoration and

rehabilitation projects dealing with reefs that were damaged by ship groundings (Gittings et al.

1988, Jaap 2000, Schuhmacher et al. 2000), dynamite fishing (Auberson 1982, Bowden-Kerby

-outbreaks (Harriott and Fisk 1988) and tourism (Rinkevich 1995, van Acanthaster plancii2003),

reeck and Schuhmacher 1999).T

The harvest of coral fragments When using coral fragments, caution must be taken in many ways:

should be as non-destructive and sustainable for the donor reef and colonies as possible. Collected

fragments have to be handled with great care, as the tissue is sensitive. Their size and the availability

of transplantation substratum are limiting factors for a positive performance: coral fragments are

able to colonize areas poorly suited for larvae colonization, such as for example sand bottoms

Their size and the transplantation technique have (Highsmith 1982, Heyward and Collins 1985).

ger . Survival rates of unsecured fragments can be increased when using larto be chosen carefully

fragments of more than 30 cm, while small sized fragments display higher mortalities (Bowden-

When small sized fragments are firmly attached to e.g. concrete nails driven in the Kerby 1997).

When choosing suitable corals for substrate, the survival rates can increase (Okubo et al. 2005).

transplantation, the life-history strategy of species should be considered: survival rates of coral

fragments with a k-mode (slow growth, as e.g. found in massive corals) strategy were observed

comparison of the Aap et al. 1992). -mode (rapid growth) species (Yto be superior to those of a r

Acrsurvival rates of ferent growth forms showed that the staghorn type species with difopora

Those had the best survival rates compared to bushy and tabular types (Smith and Hughes 1999).

fragments with multiple tips reached twice the total length compared to single-tip fragments

had a opora formosa Acrin the same time (Rinkevich 2000), and non-spawning fragments of

four times increased growth rate compared to those of bigger, spawning fragments (Okubo et al.

, even closely related species that are both dominant in the same reef area respond 2007). However

ap and Molina 2003). ferently to transplantation as well as to their new environment (Ydif

Aim of the study1.3

The aim of this thesis is to address the lack of information on peak seasons of sexual reproduction

These data will help to shed more light and reproduction cycles from equatorial Indonesian reefs.

on the question whether synchronous mass spawning is also characteristically for equatorial reefs,

9

fulfil this goal, recruitment oTor if such observations are exceptions and cannot be generalized.

The study further studies and histological techniques of coral tissue examination have been used.

attempts to test if the asexual reproduction, in terms of longitudinal length increase of coral

fragments, can be positively manipulated by the use of an electrical field. Such reef rehabilitation

measure would be helpful in areas where natural recruitment is lacking by increasing the coral

cover – both instantly and in the long term - that then could function as an attraction for and a new

source of natural recruits. Furthermore, if the corals are able to benefit from an electrical current,

as manifest in increased growth rates, it is assumed that they are able to allocate more resources

towards sexual reproduction.

Objectives of this study are to:

a) clarify if seasonal recruitment patterns in close proximity to the equator in North Sulawesi

occur

b) identify the coral families that are involved in a)

c) find evidence if mass spawning is part of these patterns

d) reveal the number of gametogenic cycles in selected coral species

e) test the hypothesis that transplanted coral fragments show increased growth rates and higher

survival due to stimulation in the vicinity of an electrical field

f) clarify whether a positive response by fragments varies among transplanted species

2. General Material & Methods

2.1 Study

eaAr

Asia encompasses approximately 30% of the world’South-East

s coral reefs (Chou 1997).

The

Indo-Pacific between the Indonesian Sumatra and French Polynesia is the global center of marine

diversity for several major taxa such as corals, reef fish and crustaceans (Bryant et al. 1998, Bruno

and Selig 2007). Its reefs had an average coral cover of approximately 42% in the early 1980s

that declined region-wide to 22% by 2003, though exceptional reefs with more than 90% coral

riangle (Fig. 1) was Tcover still can be found (Bruno and Selig 2007). In 2003 the so-called Coral

The boundaries of this outlined as a first step in a marine ecoregional conservation assessment.

area are primarily based on high coral biodiversity in countries harboring more than 500 coral

species, namely the five countries of Indonesia, East , Philippines, Malaysia (Sabah), and imorT

gest archipelago in the world, Papua New Guinea (Green and Mous 2004). Indonesia is the lar

1°S. with approximated 17,500 islands and 54,700 km of coastline stretching out from 6°N to 1

deep-water channel runs between Bali and Lombok in the south and Borneo and Sulawesi in A

10

the north and separates the country into two biological zones by a sharp biogeographic break

allace Line. It was first thought to separate only terrestrial forms from eastern and Wknown as the

s allace’Wwestern Indonesia, but new genetic studies of crustaceans give evidence for a marine

allace line, is located right in the center of WLine too (Barber et al. 2000). Sulawesi, east of the

s north-eastern coast riangle. Its northern tip, the southern Philippines and Borneo’Tthis Coral

are framing the Celebes Sea – part of an ancient ocean basin and now hotspot in an area of high

The sites studied here are all located at the far northern tip of Sulawesi in and . marine biodiversity

The Park includes reefs of the main land in around the Bunaken Marine National Park (Fig. 2).

close proximity of the provincial capitol Manado, and the islands Bunaken, Manado ua, Siladen, T

The absence of a continental shelf allows the coastal area of the park to drop Nain and Mantehage.

The depth between the islands of the park is from 200 m directly down to the continental slope.

to 1840 m (Mehta 1999).

2.2

Settlement tiles & settlement frames

, untreated and uncoated natural limestone tiles were used. For the recruitment studyThese tiles,

locally called “batu alam”, were easy to find in local hardware shops.

Fig. 1

iles were custom-cut in T

riangle with North Sulawesi TAsia showing the boundaries of the Coral Map of South-East

in middle. it

eron et al. unpublished data)SOURCE: Coral Geographic (V11

iles were recycled after examination for recruitment by sanding Tthe dimensions 15 x 15 x 1 cm.

them with a grinderAll calcareous structures, like barnacles, oysters, .

and corals’Canalipalpata

skeletons could be efficiently removed without leaving remnants behind.

The design of the frames (see Fig. 2 in Chapter 2) allowed for an alignment with one side directly

facing the water current. Furthermore, the frame design and the alignment of tiles in a 60° angle

This was done to assured that one side of the tile sets always lay in the slipstream of the current.

minimize any potential effect from changing current direction and intensity on recruitment rates.

2.3

oduction statuseprmonitoring of rIn situ

f below an expected sterile colonies were broken ofoporaAcrOn every sampling date, branches of

zone to check for their reproductive state as described in

This is an easy way allace (1985a). W

to conduct monitoring for branching corals with bigger polyps. Mature eggs, planulae or sperm-

egg bundles are usually red, pink or orange and easy visible to the naked eye due to their size in

the skeletal structure (Fig. 3).

Fig. 2

The presence of pigmented eggs is an indicator for an upcoming

Map of North Sulawesi showing the study area and the sampling sites: Meras close to the

s Point and Fukui on Bunaken and Lihage - a small island south-west city of Manado, Raymond’

The location within Sulawesi is indicated on the map in the inset.of Gangga.

12

Broken Fig. 3

fracture

f of

oporaAcr-fragment with pink coloured egg in the upper right corner of the

spawning event on or shortly after the subsequent full moon (Harrison et al. 1984, Baird et al.

2002, Guest et al. 2005a).

2.4

Histological production statusepr examination of reparation for

f with tongs or a hammer and labelled for later identification. Pieces of coral colonies were broken of

They were then immediately transferred into jugs filled with a 10 % Formalin-seawater solution

% formic 1and stored for at least one week for proper fixation. Skeletal parts were decalcified in 1

acid for up to three days, changing the solution as necessary. In many cases a total decalcification

, as tissue branches was not necessaryPocillopora verrucosaof the skeleton of the more massive

The tissue was then rinsed with f from remaining skeletal fragments. could be easily peeled of

running tap water and stored in a 70 % Ethanol solution.

For the production of histological preparates approximately 1 cm

2-quadrates of tissue were cut

They were run through a series of alcohols (80 % from the stored tissue samples with scissors.

for 1 hour, 90 % for 1 hour, 95 % for 1 hour, 96 % for  hour) for dehydration. They were then

transferred to xylene-creosote (1 hour), xylene (1 hour), paraffin-xylene (1 hour) and paraffin (at

ioho et al. 2001). least 1 hour) before finally being embedded in paraffin blocks (T

Cutting series of 6μm thickness were made through centrally located polyps and mounted on

objective slides. Slides were washed in a xylene-substitute for 10 min to solve the paraffin.

13

evaporate the xylene, the slides were dried with a hair dryer before hydrated in a series of oT

After drying, they were colored in Gill-O for 3 min). alcohol (95 % for 3 min, 70 % for 3 min, H2

hematoxylen for 4 min, transferred to H2O for 4 min, rinsed in clean H2O and dried. After 2 min of

being immersed in eosin-phloxine and being washed in 96 %-Alcohol, they were put into xylene

for 5 min before cover glasses were finally mounted with Shandon E-Z-Mount.

2.5

Surface estimation and zooxanthellae-count of coral fragments

The tissue of coral branches was removed with an airbrush gun and seawater in half-light. issue T

parts were finely ground and then seawater was added to a total volume of 40 ml. From this solution,

5 ml samples were removed and preserved with 1 ml formalin (40 %) for the determination of

. Zooxanthellae from these sub samples were counted in a Neubauer counting zooxanthellae density

The remaining 35 ml of the solution were stored in , following standard procedures. chamber

dark plastic containers and re-frozen for later chlorophyll extraction following the description of

Gardella and Edmunds (1999). Chlorophyll-a and -c concentrations were calculated according to

frey and Humphrey (1975).the equation of Jef

The blank coral skeletons were kept for surface area estimations. For this, the blank skeletal

fragments were coated in varnish to close all pores, weighted, and recoated in paraffin and

weighted a final time, utilizing the technique of Stimson and Kinzie III (1991).

calibrating A

diagram was established using objects with a known surface area and treated in the same manner

surface area was then calculated using the diagram. From The corals’as the coral skeletons above.

each of the preserved sample solutions, chlorophyll was extracted from sub-samples, as described

in Gardella and Edmunds (1999), and measured in a spectrophotometer for chlorophyll-a and -c

concentrations.

3.

3.1

General Results & Discussion

eefs: continuous with seasonal peaksoduction and settlement in equatorial rRepr

Settlement of coral spat is an important contribution for the growth and maintenance of coral

reefs and the life history of corals themselves. High numbers of coral recruits were found on

settlement tiles deployed in four reef sites in North Sulawesi (

). Recruits were found Ipaper

during every sampling interval in each site. Even if high numbers of coral recruits settle in a reef,

their mortality rate is usually high: Grazing fish (Fitzhardinge 1988), sedimentation (Babcock

ganism (Dunstan and Johnson 1998, and Mundy 1996), space competition with other fouling or

Edmunds and Carpenter 2001, Schmidt 2007) or simple settlement places with unsuitable light

14

conditions (Birkeland and Randall 1981, Maida et al. 1994) are limiting the recruitment success.

, extensive coral colonies will assure the Those recruits that remain and finally grow to healthy

survival of species and reef systems.

, the While coral settlement on the tiles in the equatorial North Sulawesi showed no clear seasonality

settlement in high latitude tropical and subtropical reefs has been found to be seasonal with months

of no, or very limited, recruitment (Banks and Harriott 1996, Glassom et al. 2004, Minton and

Lundgren 2006). Changing environmental parameters, in particular the colder water temperature,

These parameters are in direct cause the lack of recruitment during the winter season in those reefs.

relation with the reproduction time in corals. In most subtropical reefs the coral reproduction season

The reefs of North allace 1985b). Wallace and Bull 1982, falls into a warmer month of the year (W

, have a yearly average temperature of ca. 29.0 °C Sulawesi, with their close distance to the equator

Ipaperduring the dry season and 28.0 °C during the wet season (Though temperatures did drop ).

to 22.5 °C and rise to 30.1°C, these temperature extremes were only short episodes (between two

measurement intervals of 30 min) caused by interaction of strong horizontal and vertical currents

As water temperature in the tropical areas can be seen as relatively and the bathymetry of the area.

stable with minor fluctuations between seasons, it is not surprising that no clear seasonal patterns

ferences, There were seasonal difcould be detected in total coral recruitment on settlement tiles.

howeverAcroporidae and Pocilloporidae. Pocilloporid , between the most common families of

higher than those of , their total number being recruits dominated tiles throughout the year

acroporid corals (paper I). However, there were site differences in species composition on tiles and

These peaks were . distinct peaks in acroporid settlement showing a clear seasonality for this family

allace Wat variance between subsequent years and between sites as also found on other reefs (see

Though temperature might play a triggering role in the development of reproduction tissue, 1985b).

The it can be overlooked for the examined area due to the recorded minimal temperature variations.

showed II papermore detailed histological examination of coral tissue from selected species in

a single annual reproduction cycle for the broadcasting species Acropora yongei and A. pulchra.

By limiting and synchronizing the number of gamete cycles, broadcast spawning, as found in

Acroporidae, may maximize fertilization success and saturate planktonic predators, so that most

The lack of seasonality found a high proportion of the eggs survive (Oliver and Babcock 1992).

in pocilloporid settlement in the examined reefs can be explained by the dominant reproduction

. Most of its members reproduce as larvae-releasing brooders that are able strategy in this family

. Furthermore, Pocilloporidae were one of the dominating to release larvae throughout the year

families in the four stations (unpublished data), with their brooded larvae most likely to settle in

close distance from their mother colonies on settlement tiles nearbyioho et T, as demonstrated by

al. (2001). One of such brooding pocilloporid is Seriatopora hystrix (paper II), a common species

found in all examined sites. Ripe ova and spermaries were present in every examined sample

in this species. Often neighbouring polyps contained well-developed larvae at the same time,

verifying S. hystrix as a continuous brooder (paper II) and indicating that larvae of this species

15

were part of the pocilloporid recruits found year round on the settlement tiles (

Ipaper). The

has a reproduction mode less common for this verrucosa .Pother examined pocilloporid species

. Histological examination of specimens collected , as it proved to be a spawner in this studyfamily

ferent sites revealed an extended time of the year where ripe, zooxanthellae-containing in the dif

This data also showed that the North Sulawesi population has asynchronous eggs were present.

.reproduction patterns and that at least some colonies were containing ripe eggs twice a year

The relationship between the timing of coral spawning and recruit settlement has been shown in

allace 1985a, Hughes et al. 1999, Glassom et al. 2004, Mangubhai et al. a number of studies (W

2007). The peaks in acroporid settlement observed in early April and early June 2006 (paper I)

in A. pulchra in Lihage concurred with histological findings and field observations of ripe eggs in

April and A. yongei in May (paper II). The time from gamete release until settlement competency

can range from as short as 2.5 days (Miller and Mundy 2003) to a maximum competency time of

78 days (Richmond 1988), depending on the spawning species and the water temperature (Nozawa

This time range falls well into the time between histological findings of ripe and Harrison 2000).

). Furthermore, the increase in I & IIpapereggs and increase in recruit number on settlement tiles (

recruit number coincided with small temperature increases noticed by the temperature loggers tied

to the settlement frames (. Experiments with free-swimming larvae showed that sudden I)paper

fect (Coles 1985, Nozawa and Harrison 2007).increases of temperature have a signalling ef

Even if the results of paper I and II were able to show a lack of clear seasonality in coral recruitment

and an asynchronous reproduction in some of the examined species – they were not able to rule

out the existence of mass spawning based on synchrony in this equatorial region. Some of the

recruitment peaks in certain weeks of the year are in fact most likely the result of recruitment from

, uncertainties in coral recruit identification on the species level a high number of species. However

s techniques do not allow such a precise classification.remain as today’

owth of coral fragments and survivorshipManipulation to enhance gr3.2

While sexual reproduction in single colonies takes place only during certain times of the year

), the asexual reproduction in the form of budding - better known as longitudinal I & IIpaper(

growth enhancement (from hereon called “growth”) – is a continuous process without any seasonal

gy for the development breaks in between. It generally slows down when corals are using more ener

of gametes (Okubo et al. 2005) or when exposed to physical stress, as for example fragmentation.

The asexual reproduction in the form of fragmentation is a natural process that finds application

in the form of coral transplantation in reef rehabilitation and restoration projects and was tested

in . Its results demonstrated that the mineral accretion technique supports a strong and IIIpaper

secure hold of transplanted corals. Lose attachment is known to reduce coral growth and is often

the reason for loss of fragments. On the electric reef, a firm connection between fragments and

Those fragments tied to the control structures needed several substrate developed within a few days.

16

, alternativelyweeks before firm attachment or, never reached the same strength of attachment.

The present work demonstrated survival rates of up to 100% for treated fragments, depending on

The lowest survival (19%) was measured on a control structure, type of experiment and species.

where fixation of the fragments was only established by cable ties. Fragments never found the

fecting factor might have An additional afsame extreme hold as they did on the cathode structures.

been the placement of the transplantation board directly on sandy bottom, with sedimentation

causing extra stress (Crabbe and Smith 2005). Survival of fragments always is a critical factor for

the success of rehabilitation and restoration projects involving coral transplantation (Clark and

Edwards 1995). But even if survival is high, sufficient transplant growth is not guaranteed, as the

ap and Gomez 1985, Custodio III and Ymonitoring of rehabilitation projects has shown (e.g., see

The main reasons for reduced growth rates in transplants are increased stress through ap 1997). Y

handling of corals, tissue damage, size of fragments, species, and use of unsuitable techniques.

opora yongei Acrand exhibited very low growth rates in all three experiments, which A. pulchra

gy towards can be interpreted as increased transplantation stress. Fragments first must expend ener

the healing of tissue narcosis around the fracture, which often accompanies development of

gy gets redirected towards longitudinal growth. Higher amperage new polyps before the ener

demonstrated to be a stress factor as well, as those fragments that were treated with lower amperage

This is likely due to increased amounts of brucite, a rather soft form of had better growth rates.

mineral accretion with high alkalinityganisms fect many or, which has been shown to negatively af

only A. yongei (reviewed in Eisinger et al. 2005). Furthermore, total zooxanthellae numbers in

amounted to half the densities found in donor colonies, but were still significantly higher than those

ferences between treated and untreated showed neither significant difA. pulchrain the controls.

reduction of zooxanthellae densities is a good indicator A. fragments nor compared to the donor

of physiological stress in response to anomalous environmental conditions (Jones 1997a, Jones

, these results are in strong contrast to the enhanced growth and higher number of 1997b). However

zooxanthellae previously observed in the tissue of fragments transplanted onto electric substrates

(Hilbertz and Goreau 1996, Goreau et al. 2004, Goreau and Hilbertz 2005).

4. Concluding

remarks

When converting the highest number of recruits found during the final sampling period in Meras

into recruits per m

2-2 were observed. Ferse (2008) conducted a , on average, 232 recruits m

concomitant study in the same sampling site but in approximately 16 m depth, with a sampling

-2. interval of three month, and counted 363 recruits mThough data can not be compared one to

ferent sampling interval, it still demonstrates that recruitment in depth might be one due to the dif

similar increase of Ahigher than in shallower depths, where the present work was carried out.

recruitment to a depth of 20 m has also been observed by Smith (1997), who compared settlement

17

ferent depths. Howevertiles deployed at dif, the number of recruits in the present study on tiles

deployed for a duration of one year was much smaller than those on two- and three-month tiles,

indicating that a longer deployment in the water does not automatically lead to a higher number of

These findings are also supported by the results of Schmidt-Roach (2008), who compared recruits.

ferent amounts of time from Meras attached in approximately 8 m depth and tiles deployed for dif

found an increase during the first weeks but a decline in recruitment after two month of dispersal.

ferences of sampling depth and the coarser sampling interval of Ferse (2008), the Despite the dif

concomitant works noticed analogue increases of recruitment during certain times of the year: The

present study with its fine scale settlement patterns noticed an increase in the last week of June and

November 2006 as well as in the last week of May 2007 in Meras, which also could be detected on

the three-month tiles collected in June and December 2006 and May 2007 by Ferse (2008) from

bigger depth in Meras. Similar patterns were also noticeable for the neighbouring island Lihage,

August peak on August 2006 (present study), and the July/ with recruitments peaks in June and

The use of untreated limestone tiles proved to be an excellent settlement Gangga (Ferse 2008).

substrate for recruitment studies. In combination with growth keys gained from the fluorescence

census technique for the early detection of coral recruits, it was further possible to narrow the time

.of settlement down to one month with a certain degree of probability

with the preparation and following examination II paper histological work as conducted in A

of coral tissue is very work-intensive, so that the number of replicates has to be kept small.

Furthermore the chances of missing the ideal cross-sectioning of reproductive tissue are high,

with a degree of uncertainty regarding the reproductive status remaining. inspection in situ The

allace 1985a) seems to be much more suitable and branches (Wopora Acrof fracture sites from

time saving, if not even more reliable for species with big-sized polyps when only focusing on

, the predicted settlement times in combination with the development status of ova. However

observations of spawning events helped to gain a detailed in situ histological examination and

inside view of sexual reproduction patterns for these Indonesian reefs.

were in some points III paperThough the results of the mineral accretion technique documented in

disappointing regarding the previously asserted “multiple-times enhancement of coral growth”, it

still fulfilled the main requirements for a successful rehabilitation project when the “right” settings

were utilized. The fixation of the used fragments was excellent and their growth was only slightly

ferent from the controls not in direct contact to the cathode, and thus only exposed to a weak dif

likewise pattern was found in the similar high survival rates. It is clear that this Aelectrical current.

is not a “wonder tool” that will be able to save coral reefs worldwide, as in the end, transplanted

While the developers also fragments are still depending on suitable environmental conditions.

paperpromote a higher stress and bleaching resistance, the results presented in were not able III

to support this hypothesis. Furthermore, big scale projects find their limitations, as the technique

gy-consuming technical solution with the need of quite intensive maintenance, remains an ener

as cables, connections and power supply need continuous attention. It is also limited in its use in

18

Although the developers see the possibilities to remote areas where no power supply is available.

power such installations by solar panels, extra safety and vigilance would be needed in this case,

thus creating extras costs.

, due to the ease of installation and the low cost, the most expensive components of the However

ger (ca 60 US $) and anode material project being the cables (ca 70 US $ per 100 m), battery char

2), it is an excellent technique for small-scale projects. It proved to be especially (ca 100 US $ per m

suitable for dive resorts aiming revitalize their house reefs that were damaged in one way or another

and were thus not interesting enough for diving guests (personal experience). Furthermore, with

increasing environmental awareness, such resorts often try to establish underwater educational

awareness.paths by connecting diverse artificial structures to increase guests’

Concerning the assumed “enhanced” growth of transplanted corals on electrical structures, it is

possible that observed changes in growth and expansion of colonies are more likely to be noticed

on artificial structures than in the surrounding natural reef, as such structures give geometrical

The fast occupancy of free space on such structures by corals also might be a result reference points.

of normal space competition and better light regimes for all branches due to fewer competitors.

Overall, the electro-chemical deposition of minerals on conductive materials seems to have a

fect on stability of both the structures and the transplanted corals, than having higher positive ef

fects on the corals.positive physiological ef

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. Mar Biol 88: 217-233.oporaAcrthe coral genus

allace CC (1985b) Seasonal peaks and annual fluctuations in recruitment of juvenile scleractinian Wcorals. Mar Ecol Prog Ser 21: 289-298.

Wallace CC, Bull GD (1982) Patterns of juvenile coral recruitment on a reef front during a spring

summer spawning period. Proc 4th Int Coral Reef Symp 2: 345-350.

Ward S (1995) Tscleractinian coral wo patterns of enerPocillopora damicornis. Coral Reefs 14: 87-90.gy allocation for growth, reproduction and lipid storage in the

WAustralian Institute of Marine ilkinson C (ed.) (2004) Status of coral reefs of the world: 2004. ownsville, pp 264.TScience,

25

illis BL, Babcock RC, Harrison PL, Oliver JK (1985) Patterns in the mass spawning of corals on W

the Great Barrier Reef from 1981 to 1984. Proc 5th Int Coral Reef Congr 4: 343-348.

YThe case for restoration of tropical coastal ecosystems. Ocean Coast Manag 43: (2000) ap HT

841-851.

Yap HT, Alino PM, Gomez ED (1992) Trends in growth and mortality of three coral species

(Anthozoa Scleractinia), including effects of transplantation. Mar Ecol Prog Ser 83: 91-

101.

Yap HT, Gomez ED (1985) Growth of Acropora pulchra: III. Preliminary observations on the

fects of transplantation and sediment on the growth and survival of transplants. Mar Biol ef

87: 203-209.

(2003) Comparison of coral growth and survival under enclosed, semi-natural , Molina RAap HTY

conditions and in the field. Mar Pol Bul 46: 858-864.

Coral reef restoration projects in Sutthacheep M, Pettongma R (2006) ,Teemin Y

Ocean Coast Manag 49: 562-575.

Coral reef restoration projects in

. Biol Cons 92: 73-83. (2000) Restoration ecology and conservation biologyTPoung Y

Thailand

.

26

2Chapter

Determination of fine-scale temporal

oporid and pocilloporid variation in acr

settlement in North Sulawesi, Indonesia

27

First row from left to right: development

Pocillopora

Second row from left to right: development

Scale bars represent 1 mm

early stage recruit to colony

oporaAcr

early stage recruit to colony

28

ess Series (submitted)ogrMarine Ecology Pr

Determination of fine-scale temporal variation in

acroporid and pocilloporid settlement in North Sulawesi,

Indonesia

Andreas KunzmannSascha B.C. Romatzki and

emenenheitstraße 6, 28359 Bropical Marine Ecology (ZMT), FahrrCenter for T

Abstract

Spats of either brooding or broadcast spawning scleractinian corals play an important role in the

recovery and maintenance of coral reef systems.

In this study variation in settlement of corals in

a low-latitude Indonesian reef was observed. Limestone tiles were used as settlement substrate

at four sites in the Bunaken National Park and nearby reefs over a 2-year period.

iles were T

Acroporidae and Pocilloporidae recruits was The time of settlement of replaced every two months.

determined with a weekly accuracy using size-age-keys from a concomitant fluorescence study for

the early detection of coral settlement conducted in the same sites. and Pocillopora total of 4280 A

recruits were recorded on 1440 tiles. Sizes of pocilloporid recruits ranged from oporaAcr3150

Acroporidae from 0.5 to 4.9 mm. Recruits were found during each sampling 0.5 to 8.4 mm and for

period and at each site on tiles throughout the yearAbundance of pocilloporid recruits showed .

April of Acroporidae, which peaked in no clear seasonality in settlement in contrast to those of

each year and between May and June in 2006 and 2007. Settlement rates appear to be correlated

The highest average coral density per sampling period was 5.8 recruits with temperature changes.

tile

-1 -1± 0.24 ± 1.15, mean Acroporidae density (7.71 recruits tile threefold higher A(mean ± SD).

These data suggest that ± SD) compared to other acroporid peaks was calculated for May 2007.

there is a steady settlement of pocilloporid recruits in the monitored reefs while settlement for

Acroporidae showed both clear seasonal peaks and occasional settlement year around. Based on

the observation of several distinct peaks in settlement per year in successive years, it is believed

that there must be several mass spawning events.

ds: Indonesia; North Sulawesi; settlement; fluorKey wor

oductionepre; coral; rtemperatur

escence technique; seasonality;

29

Introduction

The recovery and maintenance of coral reefs depends lar

gely on the settlement of planktonic

coral larvae (e.g. Baird and Hughes 1997). Sources of these larvae are either hermaphroditic or

Accordingly gonochoritic reef corals which can reproduce sexually or asexually (Szmant 1985).

they can act as broadcast spawners or planulae-releasing brooders. Broadcast spawners release

their gametes for external fertilization of eggs followed by an extended planktonic period that

can lead to a wide-scale dispersal before settlement (e.g. Harrison and

allace 1990, Wilson W

, more recent studies also show the ability for a rapid settlement of and Harrison 1998). However

larvae (Miller and Mundy 2003) as it is commonly described for brooders (e.g. Harii et al. 2001,

ioho et al. 2001).T

fer Coral reproduction and settlement of coral larvae show spatial and temporal variations that dif

ize et al. 2005), Caribbean between regions (Fadlallah 1983). Corals in the Gulf of Mexico (V

Australia (Simpson et al. 1993) and Great Barrier Reef (Harrison et al. estern W(Szmant 1985),

1984) follow more or less seasonal reproduction patterns, while those from the northern Red Sea

aiwan (Dai et al. 1992) follow no clear seasonal T(Shlesinger and Loya 1985) or North and South

patterns. Oliver et al. (1988) recorded a decrease in reproductive seasonality and spawning

synchrony of coral species from high latitude sides in the Great Barrier Reef to low latitude reefs

of Papua New Guinea.

In contrast, recruits of brooding corals are the dominant species on settlement tiles at high latitude

reefs with a corresponding and declining rate of broadcasting spawning coral recruits (Banks and

Harriott 1996, Fautin 2002, Hughes et al. 2002, Glassom et al. 2006). Many of the equatorial and

subequatorial brooding corals, particularly in the family Pocilloporidae, follow hereby a lunar

periodicity (Fadlallah 1983).

The best-known but not yet totally understood phenomenon of annual cnidarian reproduction is

probably the synchronous mass spawning as first described from the Great Barrier Reef (Harrison

illis et al. 1985, Babcock et al. 1986), which is correlated with a temporary extensive Wet al. 1984,

increase of larvae settlement on settlement tiles shortly after (W

1988).

illis and Oliver Wallace 1985,

Earlier observations of mass spawning came explicit from regions of higher latitudes.

Their

characteristically changes in environmental parameters as water temperature and light intensity

guments for a geographical limitation of this phenomenon (Shlesinger and Loya 1985, gave ar

WHarrison and , their needs Although species develop independently from each otherallace 1990):

for suitable environmental parameters for a successful reproduction are more or less similar (Guest

et al. 2005a). More recent studies reported mass spawning corals from the low latitude reefs in

ferences in temperature or tides (Baird et al. 2001), and the Solomon Islands, which lack major dif

from an equatorial tropical reef in Singapore (Guest et al. 2002, Guest et al. 2005b).

In the present work the results of a two-year settlement study from the Celebes Sea of North

30

The Celebes Sea as part of the coral Sulawesi are presented.

riangle is one of the world richest T

areas in coral diversity (Green and Mous 2004), though least studied and most endangered.

Though 445 species of scleractinian corals from more than 58 genera and subgenera have been

counted alone in the Bunaken Nationalpark area (Mehta 1999, Donelly et al. 2002), the spatial and

temporal variability in coral settlement from this South-East

described with little data available.

Asian region is still relatively poor

The objective of this study was to investigate, a) if seasonal recruitment patterns in approximate

distance to the equator in North Sulawesi occur

if mass spawning is part of these patterns.

Material and methods

Location

, b) which coral families are involved in it and c)

This study was conducted in North Sulawesi, Indonesia in and close to the Bunaken National

total of four sites have been chosen for settlement studies (Figure 1). APark.

The north tip of

Sulawesi and its islands are affected by turbid water with strong currents, rips and up and down

All sites were f shore. streams with water depths down to 2000 m starting a few hundred meters of

within a radius of 20 km.

Fig. 1

Map of North Sulawesi showing the 4 sampling sites: Meras close to the city of Manado;

s Point on Bunaken; Lakehe on the island Gangga and the island Lihage south-west of Raymond’

Gangga.

31

The site Meras (1˚31’47.50” N; 124˚49’54.51’

’E) is located in the bay of Manado. It has an

extended reef flat of up to 100 m width, turning into a sloping fringing reef parallel to the coastline.

. Even though the City of Manado is urbidity and current are light, while visibility is often lowT

1.5 km south of the reef, influence must be low due to a mainly north-south current.

colonies are found in several patches.

s Point (1˚37’54.04”N; 124˚44’1Raymond’

1.49”E) is a drop of

oporaAcrf on the wind exposed side of

Bunaken Island in the Bunaken National Park. It is located on the entrance of a channel between

Bunaken and Manado

The current is moderate to strong with shifting directions. Coral ua. T

. colonies are compact, and Pocilloporidae are the dominating family

Lihage (1˚45’36.57”N; 125˚02’10.03”E), is a small island with an expansive reef flat and moderate

The edge of the flat goes over The reef flat starts at a depth of 1 m and descends to 12 m. current.

into a rubble slope. Acropora palifera and various Pocillopora dominate the reef.

Lakehe (1˚46’29.14”N; 125˚03’28.90”E), on the east side of Gangga island, is a small fringing

, that quickly turns into a rubble slope. reef with a thin belt of coral cover

, while the current is moderate.poor and murky

Settlement tiles

The visibility is often

Three settlement frames per site were deployed in the reefs of Meras and Raymond’

s Point from

Additional six frames were installed in the reefs of Lihage and Lakehe March 2005 to June 2007.

from June 2005 until May 2007.

Fig. 2

iles were TSettlement frame holding 3 untreated limestone tiles (15x15x1 cm) per side.

fixated with cables ties and hanging in a 60˚ angle.

32

Each frame covered four directions (Figure 2), with every side housing three settlement tiles (12

tiles frame

-1-1iles (untreated, uncoated limestone, 15 x 15 x 1 cm) were hung into T). , 36 tiles site

The space between tiles and reef bottom was approximately the frame with cable ties at a 60˚ angle.

The frames were arranged in a line at 6-7 m depth with a distance of 50 m from frame to 30 cm.

frame.

iles were replaced in two-month intervals and labeled during collection. Labels gave information T

about site, frame, and position in frame.

fects. fourth frame of identical design in each site was used to examine long-term settlement efA

Therefore tiles were left at the site for 12 months before being collected.

After collection tiles were directly transferred into bleach-solution and left for 24-48 hours, they

ganisms and then dried. were rinsed afterwards with running water to remove sand and soft or

The front- and backside of the tiles, as well as all four edges were examined with a dissecting

microscope. Each coral-recruit was photographed with a macro lens mounted on an Olympus

C5050 digital camera for later identification and measurement. Outer and inner diameters of the

recruits were either measured directly with a binocular micrometer or in scaled photos analysed

with the ImageJ photo-processing program (National Institutes of Health, USA).

Acroporidae and Poritidae (Figure 3) Recruits were categorized into the families Pocilloporidae,

Those not belonging to the three families were recognized as following Babcock et al. (2003).

more detailed categorization of recruits from this study did not seem reliable, A“other families”.

ferences of the inner diameter and skeletal morphology of the even though there are significant dif

primary polyp of Pocilloporidae (Baird and Babcock 2000, Babcock et al. 2003). Skeletons of

recruits in this study were not of high enough quality to be able to rely on the measurements taken

ferences.for the inner diameter or to identify clear dif

concurrent study focused on the early detection of coral recruits by using fluorescence technique A

(Piniak et al. 2005, Baird et al. 2006). Schmidt-Roach et al. (2008) were hereby able to establish

a general growth key for Pocilloporidae (0.24 mm week-1) and Acroporidae (0.17 mm week-1)

on settlements tiles of same material, collected from an identical depth in Meras. He measured a

a)

Fig. 3

b)

c)

Acroporidae and c) Poritidae. Notice the columella in Recruits of a) Pocilloporidae, b)

the center of the pocilloporid recruit that is missing in the acroporid recruit. Distance between

the black lines on the left of each photo is 1 mm.

33

mean diameter of 1.14 mm for

Acroporidae and 1.09 mm for Pocilloporidae at first appearance.

, a calculation of theoretical settlement time down to one week was possible with By using this key

following formulas:

Age in weeks = (outer recruit diameter – diameter at first appearance)/growth key +1a)

b) Settlement during week of year = week of tile recovery – age in weeks

If the calculated settlement time resulted in a negative number or 0, the age was taken as not older

than one week. If age resulted in a number bigger than the time of tiles in the water

, the time of

tiles in the water was taken as maximum age. If the week number felt into two month, the higher

number of days decided about month affiliation.

Environmental Parameters

isibility was measured with a Secchi-disc and salinity from water samples in 5 m depth with a V

standard refractometer (English et al. 1994). Both parameters were measured in weekly intervals

gible temperature s Point. Submerbetween December 2006 and June 2007 in Meras and Raymond’

, USA) were deployed in 5 m depth in every site and set to measure in 30-idbiTTloggers (HOBO

s could be recovered, minute intervals. In the end only incomplete data from Meras and Raymond’

because of malfunctions, and lost and stolen loggers.

Statistics

allis tests (Sokal and Rohlf 1985) were used for all settlement data Non-parametric Kruskal-W

as:

a) data were unbalanced due to stolen settlement frames occurring once in every site

b) normality could not be obtained by transformation of data.

Comparison between sites was followed by a Mann-Whitney-U-test for pair wise comparison of

7.0 (SAS-Institute, USA).All data were analyzed with JMPthe sites.

Results

Environmental Parameters

Dry season is generally from May to September (south-east monsoon), while the wet season

34

is from November to March (north-west monsoon). Salinity ranged from 30 to 32‰ in 5 m

, 2007 to as independent from season. In Meras visibility ranged from as low as 6.5 m in January

, 2006, to 14.5 m s Point from 27.5 m in December, 2007, and in Raymond’good as 28 m in May

verage temperature in Meras between December 2005 and January 2007 was A, 2007. in January

28.5˚C ± 0.6 (mean ± SD) with a minimum temperature of 22.4˚C and a maximum of 30.5˚C. On

March 3, 2006, the device logged a distinct thermocline with a temperature increase of almost 5

˚C within 30 minutes. Late June/ early July (29.0˚C ± 0.3, mean ± SD) and November/ December

2006 (29.1˚C ± 0.5, mean ± SD) were the warmest times of the year in contrast to middle March/

s Point April (27.8˚C ± 0.3, mean ± SD) and September (28.1˚C ± 0.8, mean ± SD). Raymond’

temperatures were logged between December 2005 and July 2006. Mean temperature was 28.9˚C

emperatures were T± 0.5 (mean ± SD) with a minimum of 25.8˚C and maximum of 30.5˚C.

on average 0.45˚C higher than mean temperatures in Meras (28.5˚C ± 0.6, mean ± SD) with a

minimum of 22.8˚C and maximum of 30.1˚C during this time.

axonomic pattern and recruit density in the two-month sampling period T

Acroporidae and 188 (2.5%) Poritidae recruits total of 4170 (55%) Pocilloporidae, 3107 (41%) A

13 An additional 1were found on 1440 tiles from March 2005 to May 2007 at the four sites.

ferentiation in family level. recruits (1.5%) were classified as “others” without a further dif

Pocilloporid recruits were the dominant family in all sites except Meras, which was dominated by

able 1). Lakehe showed the highest proportion of Pocilloporidae with 79 % while Acroporidae (T

Acroporidae proportion was here the lowest (19%).the

-2site ). The The number of recruits per tile ranged from 0 to a maximum of 28 (= 550 recruits m

-214 recruits mLihage had the highest average number with 5.8 ± 0.24 (mean ± SD; = 1) recruits

s Point with 4.2 ± 0.19 recruits (mean ± SD; = 82 per tile, while the lowest was found at Raymond’

Number of recruits on all examined tiles (n) per station from March 2005 until able 1.TMay 2007. Number of tiles per station is indicated by n.

LihageLakeheMeras

(n = 373)(n = 350)(n = 348)

no(%)no(%)no(%)

Pocilloporidae1297(79)1032(50)820(39)

oporidaeAcr

Poritidae

Others

317(19)948(46)1196(39)

12( 1)42( 2)39( 2)

16( 1)23( 1)53( 3)

s PointRaymond’

(n = 370)

no

874

584

94

17

(%)

(56)

(37)

( 6)

( 1)

35

other familiesritidaeoPAcroporidaecilloporidaeoP

ointymond'sPaa) R100%other familiesritidaeoP90%Acroporidae80%cilloporidaeoP70%60%50%40%30%20%10%0%-07ch-07ch-06yMay-05July-05January-06MarMay-06July-06January-07MarMaJuly-07
September-05November-05September-06November-06
b) Molas100%90%80%70%60%50%40%30%20%10%0%-07y-07rMay-05July-05January-06March-06May-06July-06JanuaMarch-07MayJuly-07
September-05November-05September-06November-06
c) Lihage100%90%80%70%60%50%40%30%20%10%0%6-05-06May-05JulyJanuaryMarch-0May-06July-06March-07May-07July-07
September-05November-05September-06November-06January-07
ed) Lakeh100%90%80%70%60%50%40%30%20%10%0%er-05er-05-07
May-05July-05bJanuary-06March-06May-06July-06ember-06March-07May-07July-07
SeptembNovemSeptember-06NovJanuary
Percentage average family distribution per 2-month tile and sampling period in each site: Fig. 4s iles were first deployed for Raymond’Ts Point, b) Meras, c) Lihage and d) Lakehe. a) Raymond’Point and Meras in March 2005 and in June 2005 for Lihage and Lakehe.36

temperature [˚C]temperature [˚C]30.029.529.028.528.027.527.026.526.025.530.029.529.028.528.027.527.026.526.025.5
MayMay-07-07temperatureAprMar-07-07AprMar-07-07
AcroporidaeFebJan-07-07FebJan-07-07
Dec-06Dec-06NovOct-06-06Nov-06
PocilloporidaeSep-06OctSep-06-06
Aug-06Aug-06-06Jul-06Jul-06Jun-06JunMayApr-06-06May-06
-06Apr-06Mar-06MarFebJan-06-06FebJan-06-06
Dec-05Dec-05NovOct-05-05Nov-05
-05OctSep-05Sep-05JulAug-05-05AugJul-05-05
a) Raymond's Point-05Jun-05Junb) Meras

Aug-05Aug-05-05Jul-05Jula) Raymond's PointMay-05b) MerasMay-05
-05Jun-05Jun-05Apr-05Apr4.03.53.02.5recruits tile 2.01.51.00.50.04.03.53.02.52.01.51.00.50.0
recruits tile -1-1s verage settlement number (mean ± SD) per week and site on 2-month tiles: a) Raymond’A Fig. 5 a&brecruits tile-1. APoint, b) Meras. Month on x-axis are divided into weeks. Notice that the last data point outside b) is 7.71 verage temperature data per week are plotted on the secondary y-axis for a) Meras from
s Point from December 2005 until Juli 2006.December 2005 until January 2007 and b) Raymond’37

c) Lihage4.03.5

3.0

2.52.01.5recruits tile -1

1.0

0.5

May-07-07Apr-07Mar-07Feb-07JanDec-06Nov-06-06OctSep-06Aug-06-06Jul-06JunMay-06-06Apr-06Mar-06Feb-06JanDec-05Nov-05-05OctSep-05Aug-05-05Jul-05JunMay-05-05Apr0.0

d) Lakehe4.0

3.5

3.0

1.52.52.0recruits tile -1

1.0

0.5

May-07-07Apr-07Mar-07Feb-07JanDec-06Nov-06-06OctSep-06Aug-06-06Jul-06JunMay-06-06Apr-06Mar-06Feb-06JanDec-05Nov-05-05OctSep-05Aug-05-05Jul-05JunMay-05-05Apr0.0

verage settlement number (mean ± SD) per week and site on 2-month tiles: c) A Fig. 5 c&dLihage and d) Lakehe. Month on x-axis are divided into weeks.

38

-2). Recruits on tiles were found during each sampling period and at each site throughout recruits m

. the year

fered between sampling periods and sites (Figures 4). Pocilloporid coral Family composition dif

recruits dominated tiles in three stations during almost every sampling period, beside the May

Acroporids. Meras was the only 2005, July 2006 and May 2007 periods, which were dominated by

Acroporids mainly dominated tiles throughout the time of sampling with an extreme site, where

peak of 90% in the July 2007 period. Exceptional periods were only in January and March 2006

when pocilloporid recruits dominated there.

Size of recruits

gest pocilloporid recruit observed was 8.0 mm after 90 days immersion (34 polyps) and The lar

Acroporidae ranged from 0.5 to 4.9 mm (1 and the smallest 0.5 mm (1 polyp). Settlement size of

polyps; 1 polyps; 90 days immersion) and for those of Poritidae from 0.5 to 3.0 mm (1 and 111

84 days).

Comparison of locations

ferent for year 1 (June Number of recruits of both families between locations was significantly dif

April 2007) (T2005 – May 2006) and year 2 (June 2006 – Acroporidae able 2). In year 1 most

able Acroporidae were found in Meras (Trecruits were found in Lihage, while in year 2 more

Acroporidae. In year 1 the highest number 3). In both years Lakehe had the lowest number of

of Pocilloporidae was found in Lakehe, which is more than double the numbers in Meras. In

the second year increased numbers of Pocilloporidae could be found in Lihage with the lowest

s Point.number in Raymond’

ference between the two years (all sites) for number of Pocilloporidae There was no significant dif

but a significant difference for those of Acroporidae (Kruskal-Wallis: 2 = 33.098, p < 0.001, df

Acroporidae could also The significant increase of . = 1), which was higher in the second year

. Consequently Pocilloporidae ferbe seen within all sites, except for Lakehe where it did not dif

Twith able 2. Number of recruits between locations was compared with Krusakal-W = 0.05 for significance for pooled years: year 1 = June 2005 until May and year 2 = June allis test
April 2007).2006 until May 2007 (for Lakehe and Lihage

year 1
Acr oporidae 3 df 187.303  < 0.001 p 3 df
3 < 0.001 3 56.284 Pocilloporidae

2year p  < 0.001 187.303 < 0.001 21.94

39

Table 3. Average number (± SD) of recruits per tile based on monthly data: June 2005 until
April 2007) May 2006 was pooled as year 1 and June 2006 until May 2007 (for Lakehe and Lihage 2{}Whitney Uas year 2. Numbers in test with  = 0.05 for significance. are converted recruit number per m. Years were compared with a Mann-

Lakehe Lihage Meras sRaymond’

Point

Acroporidae 0.19 year 1 (±0.03)
Acroporidae Pocilloporidae 1.09 2.09 (±0.13) (±0.08)
Acroporidae Pocilloporidae 1.07 1.22 (±0.06) (±0.07)
Acroporidae Pocilloporidae 0.57 0.97 (±0.04) (±0.07)

(±0.06) 1.15 Pocilloporidae

year 2 df 2 p
1.17 0.61 (±0.07) (±0.08) 1 1 19.171 26.986 < 0.001 < 0.001
1.37 1.28 (±0.07) (±0.09) 1 1 1.528 0.342 0.217 0.559
0.94 1.79 (±0.06) (±0.15) 1 1 2.779 23.055 0.096 < 0.001
0.009 6.844 1 (±0.08) 0.77

1 (±0.09) 0.90 0.370 0.803

showed a significant decrease in Lakehe for the second year (Mann-Whitney comparison of pairs: < 0.001).pComposition of both families in terms of settlement number within locations was significantly

ferent: Pocilloporidae were dominant in every site for both years (Mann-Whitney pair wise difcomparison: fer < 0.05) with the exception of Meras in year 1 when families did not difp < 0.001).pAcroporidae in year 2 (Mann-Whitney: , but were dominated by significantly

Fine-scale temporal settlement patterns

Acroporidae and Pocilloporidae recruits in one-month intervals was possible after comparison of Aference between months The difapplying the established growth key (Schmidt-Roach et al. 2008). for Acroporidae as well as Pocilloporidae was significant in every site and every year (Kruskal-Wallis; p < 0.005). Seasonal peaks of Acroporidae were reached in May 2005 in Raymond’s Point
Additional peaks were April and June 2006 in all sites. (Figure 5a) and Meras (Figure 5b) and in April 2007 for Lihage (Figure 5c) and Lakehe (Figure 5d), while settlement started to found in

s Point a month later in May 2007. In Meras during the final increase in Meras and Raymond’-1, sampling period in May 2007, the theoretical acroporid settlement (7.71 ± 1.15 recruits tile

mean ± SD) was three times higher than any of the previous acroporid peaks (max 2.75 ± 0.61

-1recruits tiles Point was more At the same time settlement in Raymond’, mean ± SD) observed.

-1, mean ± SD) to previously observed peaks (max 0.78 ± than doubled (1.97 ± 0.79 recruits tile

-1The highest number of pocilloporid recruits was counted on the , mean ± SD). 0.2 recruits tileAugust 2005 tiles in Lakehe with 3.13 ± 0.09 (mean ± SD). Distinct seasonal settlement patterns for Pocilloporidae could only be seen for Lakehe (August and October 2005 and 2006, with an

40

additional peak in May 2006), while the other sites showed no clear seasonal patterns for this family. Pocillopora settlement numbers seemed to decrease from 2005 to 2006, while Acropora
numbers increased during that period.

Orientation of recruits on tiles

2) was higher Although the number of recruits on the backside of the tiles (surface area = 225 cm2), the theoretical number after transformation to equal than on the edges (surface area = 15 cm2ferent trend: 79.57 % of all recruits would have been on the ) showed a difsurface areas (1 mThe lower edge of the tile, followed by the backside with 9.35 % and the lateral sides (4.35 %). tile frontside (2.92 %) and the upper edge (3.81 %) were the places with the lowest recruitment. Acroporidae and Pocilloporidae recruits were identical for Settlement preferences (Figure 6) of Acroporidae preferred the Therefore ferences. the front- and backside of tiles with only minor difmore shaded upper and lower edges, while Pocilloporidae were more frequently found on the lateral edges. Poritidae never settled on the upper edge and were rare on the tile front side (0.6 %). 89.3 % of all “other families” were found on the lower edge but never on the lateral edges.

100%

90%

80%

70% 60%coral family distribution50%40%30%

20%

10%

0%

cilloporidaeoP

Acroporidae

ritidaeoP

other families

sidesupper edgelower edgefrontsidebackside

Percentage distribution of coral recruit families on 2-month tile surfaces displayed as Fig. 6pooled data for all sites.

41

3.5a) Raymond's Point32.5-12recruits tile 1.5

1.510.5

00-11-22-33-55-1010-1515-20>20
3c) Lihage2.5

2recruits tile 1.51

0.5

3b) Meras2.5

2

1.51

0.5

00-11-22-33-55-1010-1515-20>20
3other familiesd) LakeheritidaeoPAcroporidae2.5oPcilloporidae

2

1.51

0.5

000-11-22-33-55-1010-1515-20>200-11-22-33-55-1010-1515-20>20
size category in [mm]size category in [mm]s Distribution of recruits in size classes and families on 1-year tiles for a) Raymond’ Fig. 7Point, b) Meras, c) Lihage and d) Lakehe.

Settlement on 1-year-tiles-2An average of 9.8 ± 2.8 (mean ± SD; 190 recruits ms ) were found on 1-year tiles in Raymond’-2) in Meras (Figure 7b), 5.7 ± 0.6 (mean ± Point (Figure 7a), 3.4 ± 0.8 (mean ± SD; 67 recruits mSD; 112 recruits m-2) in Lihage (Figure 7c) and 1.9 ± 0.3 recruits (mean ± SD; 37 recruits m-2) in
Lakehe (Figure 7d). Newly and very small recruits were rare on all tiles. Percentage distribution Acroporidae 25%, 0.5% for Poritidae and of Pocilloporidae on all 1-year tiles was 58.7%, for 15% for all unidentified corals. Pocilloporidae coral recruits dominated at all sites, while Poritidae s Point counted also the higher number of big s Point. Raymond’was only recorded in Raymond’sized recruits. Encrusting Bryozoa were the dominant space competitors on every tile and at every

42

site, covering most of the tiles surfaces, followed by Bivalvia, Balinidae and Canalipalpata in

descending order of importance.

Discussion

Retrospect on methods

Laboratory experiments showed that species identification due to distinctive morphological

characteristics of newly settled pocilloporid recruits of known age and source of origin is possible

(Babcock, 2003). Crucial identification character hereby was the size of intact skeletons of the

primary polyps. Recruits in the present work were not identified to such a level, as the quality of

Therefore the diagrams high portions of examined skeletons did not allow a reliable identification.

of weekly settlement (Fig 5), that assumes an average start size rather than considering the latter

ferences between species, can be a source for errors. By interpreting the peaks mentioned size dif

on a monthly basis, these errors should be small.

While counting recruit skeleton it was furthermore expected, that they were from recruits still

alive when tiles were harvested. Consequently the age determination of recruit skeletons has to be

interpreted with caution as these “skeletal fingerprints” remain on substrate although the animals

are already dead for days or weeks (Harrison and

settlement.

AcroporidaePocilloporidae vs.

Wallace 1990) distorting the actual time of

The majority of pocilloporid corals are known to release brooded larvae while acroporid corals

are generally characterized as broadcast spawners, however there are exceptions:

Acr is a spawner (Sier and Olive 1994) while species like verrucosa

Pocillopora

opora brueggemanni from the

The larvae of broadcast spawning acroporid subgenus Isopora are brooders (Okubo et al. 2007).

corals are reported to dominate the coral spats composition in tropical reefs (Baird and Babcock

The present study is in contrast to previous findings, as spats of the genus Pocilloporidae 2000).

dominated here the majority of all tiles. Furthermore pocilloporid spats were found year around in

all sites, so that a lack of recruits was more the exception than the rule, this also concurs with an

equatorial settlement studies from Kenya (Mangubhai et al. 2007).

The pocilloporid percentage

of spats on the 2-month and 1-year tiles were also higher than those of pocilloporid spats found

ference could be , the dif. Howeveron 6-month tiles in Komodo (Fox 2004), south of the Equator

explained due to uncertainties in species identification to some degree.

There fore the acroporid

percentage on 1-year tiles in the present study is comparable with the Komodo findings.

twofold higher number of pocilloporid recruits with distinguishable temporal patterns as found A

43

As Lakehe is also a site with low in Lakehe is in direct contrast to the other examined sites.

coral cover and diversity it is possible that most larvae came rather from a specific pocilloporid

ioho et al 2001). Settlement number peaked in 10 species close by than from multiple species (T

to 12 weeks intervals and this intervals fit well into up to 6 annual reproductive cycles for some

Therefore histological examination will brooding pocilloporid corals (Stoddart and Black 1985).

be necessary to elucidate the reproductive mechanism and number of annual gametogenic cycles

of the dominating pocilloporids.

The abundance of Acroporidae showed in contrast to Pocilloporidae a clear seasonality in settlement

April, between May and June as also in November of in all sites with peaks in the months of

2006. In the present study from north of the Equator the abundance patterns in Pocilloporidae are

Acroporidae in present Therefore identical with those in Komodo south of the equator (Fox 2004).

study were spawning during both monsoon seasons, with higher settlement rates during the SE-

These -monsoon. monsoon, while acroporid abundance increased in Komodo during the NW

contradictory findings might be a direct result of high spat mortality and the cruder sampling

interval in Komodo to the present weekly settlement data.

Acroporidae which were found sporadically in other months than the peak season, were Those

) were identified as part A. palifera and A. brueggemannifound in sites where isoporan corals (e.g.

. Furthermore planulae in difof the local coral communityferent development stages were found

colonies during weekly A. brueggemannif branches of various in fractures from freshly broken of

oporaAcrchecks (Romatzki, pers. observation). Both findings give strong evidence that isoporan

are a possible larvae source.

Fine-scale settlement and field observations

The calculated times for settlement with the help of family growth keys are rather approximate

values, not exactly reflecting the exact time of larvae and gamete release. Nevertheless these times

correspond to direct spawning observations of Acropora yongei and A. pulchra in the first week

of May 2007 in Lihage (Romatzki, pers. observation). Both species coexisted in a single stand

with the dimensions 15 by 30 m. Spawning occurred during two subsequent nights, four and five

days after full moon. Patchy spawn slicks floating on the surface, as also drifting eggs in the water

column were witnessed in front of the neighbouring island Gangga. It is unlikely that all observed

Therefore it is more probable that eggs originated from the prior described single coral stand.

colonies and species in diverse locations were spawning synchronous during that oporaAcrvarious

Three weeks later an extreme increase in acroporid settlement was event and in subsequent nights.

s Point. noticed on tiles in Meras and Raymond’ occurred in these A. yongeiAs adult colonies of

was not present at all, it suggests that also here several A. pulchra, while sites just sporadically

other acroporid species were involved, contributing to additional evidence of mass spawning.

44

Settlement competency and physical factors

It is highly likely that these recruits were coming from the particular spawning night as several days

The . pass between spawning, egg fertilization, planula development and settlement competency

time from gamete release until settlement competency can range from as short as 2.5 days (Miller

and Mundy 2003) to a maximum competency time of 78 days (Richmond 1988) depending on the

broadcast spawning species. For brooding species the time of settlement competency can even be

damicornis Pocilloporaas long as 103 days (Richmond 1987), though larvae of brooding were

found in close proximity to the parent colonies, indicating settlement immediately after release

ioho et al. 2001). Nevertheless, the mass of larvae from specific T(Stoddart and Black 1985,

species follows a distinct rather than a continuous settlement pulse (Miller and Mundy 2003).

ilson and Harrison 1998) fit Maximum settlement rates between 10 and 32 days after spawning (W

well into the above observations of spawning event and sudden increase in settlement.

Furthermore the simulations demonstrated that positive buoyant particles could stay well within

a reef area for up to 20 days (Black 1993), although the ultimate settlement site for free drifting

ater that flows W, interaction of reef and current. , weatherlarvae depends on the bathymetry

along a curved or uneven coastline or object may separate from it and generate an eddy likewise

s Point might The reduced rates of coral settlement in Raymond’gier 2003). retaining recruits (Lar

be explained due to its exposure to strong currents. Located in the channel between Bunaken und

ua, currents are strong during intermediate periods but calm during tides. In combination TManado

, allowing settlement of planulae with the reef topography (see description of the site) shelter

, water flow does negatively influence the settlement rates for some might be limited. Moreover

fected brooding species (Harii and Kayanne 2002), although settlement of other species is not af

by it. However swimming speed of planula is too slow to headway against more rapid horizontal

-1 currents, though swimming speed would allow substantial vertical migrations of up to 1 m h1

Also if currents can reduce the actual settlement success on a short (reviewed in Hodgson 1985).

temporal range, they also can be an advantage for those corals that manage to settle under such

conditions. Currents can support the removal of sediment both from the coral surface and the reef,

encounter rate of zooplankton and dissolved nutrients uptake, modulating physiological processes

as enhancing the photosynthesis by symbiontic algae and increasing the respiration rates of coral

This would explain the twofold higher settlement number tissue (reviewed in Sebens et al. 2003).

s Point in comparison to the 2-month tiles and 1-year tiles of all other on 1-year tiles in Raymond’

These sites were either more current protected or more exposed to anthropogenic influences sites.

s Point. than Raymond’

fects physiological processes during all life-history stages. It is well known that temperature af

In case of planktonic larvae their respiration and metabolism rates are increasing with higher

Ytemperatures (Maldonado and increased their respiration Porites luteaoung 1996): Larvae of

significantly when exposed to a small temperature change in the range from 26.8˚C to 29.7˚C

45

(Edmunds 2005). Settlement competency as discussed above is seen to be directly related to the

gy reserves a larvae has (Richmond 1987), so that high metabolism rates can lead to a shortage ener

gy and with that to a shortened competency time (Edmunds et al. 2001). Furthermore of ener

increasing temperatures may modify the selective value for larvae to settle in specific locations.

ferent species , larvae settlement is greater at higher temperatures whereas larvae of difHowever

are adapted to species specific and narrow temperatures ranges. Post-settlement of larvae can

fected if these temperature ranges are exceeded for a prolonged time (Coles be negatively ef

1985, Nozawa and Harrison 2007). Settlement rates in Meras of both, acroporid and pocilloporid

spats followed temperature changes in either direction: dropping temperatures were followed by

This efregressive settlement rates and increasing settlement followed raising temperatures. fect

April until June 2006 when steadily increasing mean temperatures from was most apparent in

As earlier Acroporidae. 27.8˚C to 29.4˚C were overlapping with increasing settlement rates of

and later parts of the logger data are lost, it will remain subjective if settlement rates consequently

. Nevertheless, with the followed a temperature increase, making further assessments necessary

hourly high-frequency temperature variability as measured in present sites, rapid temperature

increases in certain ranges are suggested to have a trigger effect on larvae settlement.

, by summarizing the previous results it can be said that the examined sites were served Finally

with coral recruits from both, seasonal as well as continuous monthly events. Spats from broadcast

, while brooders were spawning species were more seasonally present in specific months of the year

abundant year around. Overlapping of monthly and seasonal settlement patterns lead to intensive

ime T. settlement peaks that could be backtracked with some accuracy to specific weeks of the year

and intensity of settlement in combination with spawning observation indicate mass spawning and

a high potential of self-seeding in the examined reefs. Furthermore there is presumptive evidence

that intensity of settlement followed seasonal temperature changes and is triggered by impulsive

changes to higher temperatures.

Acknowledgments

would like to thank C. Muller and G. Davi for their hospitalityeW

f of Froggies Divers, , all staf

Bunaken and Gangga Spa and Resort for all support in the dive logistics. further more would eW

like to thank S. Ferse and S. Schmidt-Roach for help in the field and S. Mangubhai for helpful

This research was supported by a DAAD (German comments on the manuscript.

Exchange Service) scholarship for doctoral candidates.

Academic

46

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49

3Chapter

scleractinian Gametogenesis of four

corals in the Celebes Sea

50

51

1th International Coral Reef Symposium (submitted)oceedings of the 1Pr

Gametogensis of four scleractinian corals in the

Celebes Sea

Andreas KunzmannSascha B.C. Romatzki and

rCenter for Temenenheitstraße 6, 28359 Bropical Marine Ecology (ZMT), Fahr

Abstract

Spatial and temporal variability in reproduction of equatorial coral species is still relatively

This study examined the mode and timing of reproduction in common species of undescribed.

North Sulawesi, Indonesia. Samples from

Pocillopora verrucosa, Seriatopora hystrix, opora Acrpulchra and A. yongei were collected in 2-weekly intervals between June 2005 and May 2007. All

collected samples were examined for their gametic cycle by using standard histological examination

The presence of zooxanthella in to quantify the gonad development stage.

.P verrucosa eggs

indicated a biannual reproduction cycle with spawning periods between January until March and

produced larvae all year round with planulae present in every month. S. hystrixAugust. June until

April 2006 and March 2007, while in A. pulchraEgg-sperm-bundles were found annually in

contained such bundles in May 2006 and 2007 when spawning was also witnessed. yongei

ds: Indonesia; scleractinia; gamaetogenesis; equatorialKey wor

Introduction

Investigations on coral reproduction have been conducted throughout the world, revealing a

A.

variety of reproduction modes, patterns and timing between, but also within, geographical regions

While the majority of coral species found in the (Sammarco 1985, Richmond and Hunter 1990):

Indo-Pacific reproduce as broadcast spawners, those in the Atlantic are predominantly brooders

The majority of corals from high latitude reefs tend to have a allace 1990). W(Harrison and

seasonal reproduction schedule, whereas with decreasing distance to the equator clear schedules

are blurring: Oliver (1988) measured a breakdown in reproductive seasonality and spawning

synchrony of coral species from high to low latitudes so that the breeding season is hypothesized to

52

be protracted near the equator (Harrison and allace 1990). Latitudinal variation in reproduction W

time has also been recorded on the species level for

oporaAcr-around in lower latitudes (Kojis 1986). in higher to year

(

Isopora), changing from seasonal

Species also show variability in the number of reproduction cycles: brooders often release

planulae multiple times per annum, while the most common pattern in broadcast spawners is

, biannual and multiple spawning single annual spawning of colonies (Fadlallah 1983). However

of some broadcasting species was also reported (Stobart et al. 1992, Mangubhai and Harrison

2008).

The common cues for timing and synchronisation of coral reproduction are seen in environmental

ferent scale, including water temperature parameters. Each of them is suggested to work on a dif

and solar insulation for the season or month (Shlesinger and Loya 1985, Penland et al. 2004),

tides for the day of the month (Harriott 1983) and light intensity for the time of the day (Harrison

et al. 1984). Although species develop independently from each other

, their needs for suitable

Their simultaneous . environmental parameters for a successful reproduction are more or less similar

response – with the extreme found in the annual mass spawning in the Great Barrier Reef - is

allace Wseen as a result of strong selective pressure promoting fertilization success (Harrison and

e 1Figur

Map of North Sulawesi showing the four sampling sites: Meras close to the city

s Point and Fukui on Bunaken and Lihage - a small island south-west of of Manado, Raymond’

Gangga.

53

1990). Further evidence for this hypothesis is seen in the absence of mass spawning events in

the northern Red Sea, with its relatively constant environmental conditions (Shlesinger and Loya

1985). However, mass spawning corals have been observed in the low latitude Solomon Islands

(Baird et al. 2001) and in a Singaporean equatorial reef (Guest et al. 2002), which both have only

minor fluctuations in environmental parameters. Based on these findings Guest et al. (2005a)

gues that mass spawning is more the result of reproduction success through synchronisation, than ar

it is of environmental parameters; and with that it is as likely to occur in equatorial assemblages,

as it is at higher latitudes.

Data on the gametogenesis of numerous coral species and precisely predictable dates of their

spawning are available for many areas in the Caribbean, Gulf of Mexico (e.g. McGuire 1998,

VBeaver et al. 2004, Bastidas et al. 2005, ize et al. 2005, Schloeder 2007) and the Vize 2005,

illis et al. 1985), but not much data is available from Wallace 1985, WGreat Barrier Reef (e.g.

s coral reefs Asian reefs, even though this region encompasses almost 1/3 of the world’South-East

(reviewed in Guest et al. 2005b) and more than 75% of all known scleractinian corals. Hereby

the reefs of North Sulawesi, Indonesia lay in the centre of this coral diversity hotspot (Green

and Mous 2004). Despite the importance of the area, in terms of its worldwide outstanding coral

omascik et al. 1997, T, very little is known about its coral reproduction and timing (e.g. diversity

Bachtiar 2000, Crabbe and Smith 2002, Zakaria 2004).

In this paper we examine the gametogenesis of four selected scleractinian species for their timing

and a possible seasonality in an equatorial reef. Histological examinations of common brooders

and spawners from these reefs were used to reveal their gametic-cycles.

Methods

The study has been conducted in North Sulawesi, Indonesia (Fig. 1). Samples of four common

scleractinian coral species were collected from four sites in approximate distance to the Equator

s Point in a two-weekly and Lihage , Meras and Raymond’able 1). Fukui was sampled in a weekly(T

Three branches were taken repeatedly from the same tagged colonies on in a five-week interval.

S. hystrixeach sampling date in a depth of 6 m ( was collected in 30 m).

Samples were immediately fixated in 10% Formalin with seawater for at least a week, decalcified

1% formic acid for up to three days with the solution changed when necessaryin 1

, rinsed

The tissue preparation for histological with running tap water and then stored in 70% Ethanol.

Tioho (2001). Texamination followed standard procedures as described in issues were stained

m thick and examined by issue slides were cut 6 Twith Gill-Hematoxylen and Eosin-Phloxin. 

. Development condition of gonads was determined following Szmant-Froehlich et al. microscopy

(1985) with slightly modified criteria for each species: Four development stages were classified

by criteria such as the geometric mean diameter [square root (greatest x least diameter)] and

54

Figure 2 Cross section of a = mesenterial filament, nc = nucleus, vc = vacuole, sp = spermaryPocillopora verrucosa polyp. ms = mesenteria, mf , oo = oocyte

were based on the presence of morphology of oocytes and testes. Further criteria for stage IV

oocytes (Hirose et al. 2001), when eggs were packed together into verrucosa.Pzooxanthellae in

bundles in A. yongei and A. pulchra or planulae presence in S. hystrix.

Results and Discussion

was found to be a hermaphrodite spawner with ovaries Pocillopora verrucosaIn North Sulawesi

This concurs with most literature findings, with the exception and testes in the same polyp (Fig. 2).

of one observation from Enewak, where has been reported as a brooder (Stimson verrucosa.P

oocytes, while stage I was rarely found 1978). Samples of each month contained stage II, III and IV

The lack of stage I oocytes might be a result of a very short-lived stage, as was formerly (Fig. 3).

hypothesized by Kruger and Schleyer (1998). Comparative data of mature egg size showed a

diameter range from 53.5m ± 15.7 in the Maldives (Sier and Olive 1994) to approximately 150 

Africa (Kruger m estimated in the Red Sea (Fadlallah 1985, Shlesinger and Loya 1985), South 

, oocyte size in this study ranged from and Schleyer 1998) and Japan (Hirose et al. 2001). However

m, with a pre-spawning average size (stage IV) of m to a maximum of 158 a minimum of 12 

Although spawning could never be witnessed, a presence of zooxanthellae in m ± 15 (n=58). 10 1

55

Overview of collected specimen at the four sampled sites. For each sample three able 1Tpolyps were examined by using standard histological methods.

Location collected Species Coordinates examined

Meras (Manado Bay) 1˚31’47.50” 124˚49’54.51”E N

Raymond’(Bunaken Island) s Point 124˚44’11˚37’54.04”N 1.49”E

1˚45’36.57”N Fukui 124˚44’23.39”E (Bunaken Island)

1˚45’36.57”N Lihage Island 125˚02’10.03”E A.

P verrucosa . n A. yongei

verrucosa .P A. yongei

verrucosa .P S. hystrix

verrucosa .P A. yongei pulchra

samples No

n = 17749=

n = 284n = 87

n = 165n = 129

n = 94n = 78n = 41

.P oocytes indicated an imminent spawning. Oocytes showed to take up zooxanthellae verrucosa three to four days prior to the spawning date (Hirose et al. 2001). Despite the fact that stage IVable 2). oocytes were found in numerous months, those containing zooxanthellae were limited (TSamples containing zooxanthellae were found one to three days prior to a New Moon, but never before a Full Moon. These findings basically fit into the reports that were identifying P. verrucosa
as a spawner around New Moon (Fadlallah 1985, Shlesinger and Loya 1985, Sier and Olive 1994, Kruger and Schleyer 1998, Hirose et al. 2001). The presence of zooxanthellae in Table 2 also show that P. verrucosa in North Sulawesi spawns
, as also reported in several other species more than once per annum with two cycles most likely, in this (Richmond and Jokiel 1984, Stobart et al. 1992, Mangubhai and Harrison 2008). Howeverstudy it could not be clarified if it is a feature of single colonies or reflects asynchrony between Asynchrony of multiple colonies within a population, as the data of tagged colonies was limited. ferent sites, while just separated by less spawning periodicity between the populations of the dif-month intervals than 30 km, was shown during some months. Spawning seemed to occur in four. Inconsistent reproduction in three sites, while in Lihage a tendency to 5 months was more likelyferent morphs within the same location are known patterns between closely located sites, or dif (Fan et al. 2002, Lin 2005). Pocillopora from closely related, but brooding Patches of Acropora yongei and A. pulchra were forming together a dense single coral stand
samples were collected in Lihage, A. pulchraWhile all of approximately 15 x 30 m in Lihage. s Point and Meras. were also collected from tagged colonies in Raymond’yongei A. samples fromm (Fig. 4). Ripe m to 290 Oocyte diameter of both species had an approximate range from 20 

56

oocytes in

A. pulchra

thbefore full moon on 6

were packed in egg-sperm-bundles found on 19

th of March and one week

As the March sampling occurred one week after full moon and April 2006.

April is suggested eggs, April sampling contained a bigger portion of stage IVas the consecutive

th May 2006 in to be the spawning month for 2006. Ripe egg bundles were also found on the 15 A.

f branches on visual census of freshly broken ofA samples two days after the full moon. yongei

ththe 5

A. yongei May 2007 in Lihage revealed egg-sperm bundles in colony patches. Synchronous

th and spawning in these multiple patches was observed four and five days after full moon on the 6

7

thThe bigger event took place in the first night and encompassed the entire coral stand. May 2007.

e 3Figur

Pocillopora verrucosa: Diameter and development stage of oocytes (top) and

April has not been sampled.spermaries (bottom) for each sampling month. Notice that

57

Table 2 Overview of Pocillopora verrucosalikely or close to spawning times in accordance to zooxanthellae in oocytes, oocyte diameter sampling dates and locations for the most ,
lunar condition and development stage. NM = new moon, FM = full moon, + = number of days after lunar phase, - = number of days before lunar phase, y = yes, n = no

Lunar condition zooxanthellae Location Sample date

13 Feb 2006 Lihage

s Point Raymond’26 Feb 2006

Meras, Fukui 26 Mar 2006

s Point Raymond’28 Jun 2006

Fukui Aug 2006 21

Meras Aug 2006 21

Lihage Aug 2006 15

Lihage 09 Jan 2007

n

y

y

y

y

y

n

n

FM-1

NM-1

NM-3

NM+3

NM-2

NM-2

NM-8

NM-8

mean sizeoocyte stage

3

4

4

4

4

4

3

3

76±4.18

13±12.31

18±7.51

1.5107±1

1±2.511

106±7.4

95±4.7

76±13.8

Such a split spawning in corals over consecutive nights is suggested to be the result of a delay in

oocyte maturation caused by variation in trophic conditions of individual polyps, due to the lower

As maturation status must have light intensity in shaded colony areas (Shimoike et al. 1992).

changed in present observation within a day from “not ready” to “ready to spawn”, a variation

arrant in concentration of sex steroid or pheromones in the water as potential spawning triggers (T

, no further mature eggs were found in tissue samples . However2005) seems to be more likely

of other months, pointing into an annual reproduction of the examined colonies of both species

Therefore a conclusion on the population level needs more quantitative data, in North Sulawesi.

ferences in within-population reproductive synchrony or split spawn as regional and annual dif

oporaAcrevents in consecutive months are common in (reviewed in Baird and Guest 2008).

polyps contained often one oocyte surrounded by one pair of spermaries. opora hystrixSeriatr

Occasionally two equal sized oocytes were located in one polyp. Oocyte size ranged from 25 to 233

m in diameter, while spermary diameter ranged from 10 to 182 m. The single planulae findings

, staying in contrast to regularly m in present studyper polyp with a maximum diameter of 408 

m in the southern Great Barrier findings of two planulae per polyp with a size of 633 ± 12 

anner (1996) defined planulae as mature when mesenteries were visible. Tanner 1996), Reef (T

In present study mesenteries were visible despite the smaller larvae size. Planulae were present

year around (Fig. 5) in examined colonies with no sign of seasonality in contrast to Hawaii and

anner 1996) where planulation showed Enewetak (Stimson 1978) and in the Great Barrier Reef (T

, from stage I S. hystrixferent development stages in . However sexual products of difseasonality

oocytes to planulae, were found simultaneously in almost every examined colony during every

sampling month. The overlapping of gametic cycles in combination with findings of empty polyps

ferent lunar phases gives evidence for planuale release without any lunar periodicity as during dif

58

A. yongei

A. pulchra

e 4Figur

pora yongeiDiameter and development stage of oocytes for each sampling month for

Acro-

April 2007 was not sampled, but spawn- (bottom). Notice that A. pulchra (top) and

was observed in beginning of March 2007. A. yongei ing in

59

MM

MAAADAA

JJJJJ

2006

S

S

OO

N

N

D

JD

J

2007

F

MFM

Figure 5 Size of Seriatropora hystrix planulae and when the were found per sampling for
March 2006 and ending with March each sampling month. Letters stay for month starting withV2007. ertical lines indicate Full Moon.

anner (1996).Talso found by Stimson (1978) and

However, their studies were conducted in subtropical waters, where water temperature changes

between seasons, while specimen in the present study were collected in 30 m depth in equatorial

emperatures measured in a nearby Twaters, where average water temperature is relatively stable.

station over a one-year period from December 2005 until January 2007 in 5m depth were ranging

between 27˚C and 29.5˚C. Hereby March and September were the coldest months (average 28˚C)

Though studies with spawning species with June and December being the warmest (average 29˚C).

proved an important role for seasonal temperature changes to trigger the gametic cycle (Jokiel et

al. 1985), such changes are not essential for this yearcontinues reproduction , that-around brooder

even when maintained at constant temperatures as shown in aquaria (Petersen et al. 2007).

The presence of zooxanthellae in P. verrucosa eggs and egg-sperm-bundles found in A. pulchra

are both indicators for an imminent spawning. Based on these indicators all three A. yongeiand

S. hystrix. Planulae of the brooding species spawning species showed some degree of seasonality

found during all lunar phases and in all month of an entire sampled year gives evidence for a

-around brooding period in North Sulawesi.year

60

Acknowledgments

like to thank Froggies Divers and Gangga Island Resort & Spa for their continuous support eW

Tin dive logistics, E. ambajong for letting us use his private lab and for help in the histological

A. Baird for useful comments on the interpretation of the tissue Juterzenka and .preparation, K. v

slides.

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. Mar Biol 88: 217-233.oporaAcrthe coral genus

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63

Chapter 4

Determining the influence of an electrical

field on the performance of

transplants: Comparison Acropora

of various transplantation

esstructur

64

65

Journal of Experimental Marine Biology (submitted)

Determining the influence of an electrical field on the

transplants: Comparison of Acroporaperformance of

various transplantation structures

Sascha B.C. Romatzki

emenenheitstraße 6, 28359 Bropical Marine Ecology (ZMT), FahrrCenter for T

Abstract

The mineral accretion method is a reef rehabilitation tool that uses the principle of electrolysis to

precipitate minerals from seawater in the form of limestone as settlement- and transplant substrate

on conductive metal racks. Previous observations indicated that the resulting electrical field

fects on corals transplanted onto the cathode-structures. had positive side efThis study aimed

to examine the impact of the direct contact with the cathode and the electrical field on growth,

oporaAcrsurvival, chlorophyll concentration and number of zooxanthellae on two transplanted

transplants showed significantly lower growth rates when the cathodic opora yongeiAcrspecies.

surface exceeded 1.67 mA

-2ged metal in comparison or when in direct contact with the char

transplants opora pulchraAcrto a lower amperage treatment or untreated control fragments.

demonstrated contradictional results between the experiments with a tendency to lower growth

rates when electrically treated. The number of zooxanthellae and chlorophyll c concentration in

zooxanthellae A. pulchra fragments was significantly higher than in controls. In A. yongeitreated

ference between treated and untreated fragments but higher chlorophyll density showed no dif

c concentration in treated fragments. Survival rates of transplants for A. yongei and A. pulchra

were in all experiments high but showed significantly lower survival when exposed to a high

demonstrated to be the more sensitive species for transplantation work. A. pulchraamperage.

Previous reports on significantly increased growth rates due to electrical stimulation could not be

supported for the here examined species.

Keywords:

ophyllchlor

coral transplantation; coral growth; mineral accretion technique; zooxanthellae; 66

Introduction

oung going dramatic growth (YThe fields of conservation biology and restoration ecology are under

s coral reefs are decreasing at an accelerating rate (Precht and Dodge 2002, 2000) as the world’

ilkinson 2004). In addition to the traditional measures of protecting, managing and conserving W

marine habitats, such engagements as reef-restoration and rehabilitation which manipulate reef-

eemin et al. 2006) are Ytopography directly (Jaap 2000, Fox and Pet 2001, Nonaka et al. 2003,

fort aiming to bring back a pre-disturbance . Hereby “restoration” is an efbecoming more popular

state (Precht 1999), while “rehabilitation” is the act of partial or full replacement, or substitution

of alternative qualities or characteristics, of an ecosystem (Edwards 1998).

In the past, various materials such as bottles, ships and car tires have been deployed in benthic

altemath and Schirm 1995, Pickering et Wzones in an attempt to rehabilitate reefs (reviewed in

These materials turned out to be, in many cases, unsuitable due to their mobility and al. 1998).

ganisms as well leaching of toxic substances. In turn, very limited settlement of marine sessile or

as low survival rates of transplants was recorded.

newer approach in coral reef rehabilitation and transplantation is the mineral accretion method A

reeck and Schuhmacher 1999) utilizing the T(Hilbertz et al. 1977, Hilbertz and Goreau 1996, van

principle of seawater electrolysis. Sea water electrolysis is characterized by a direct current (DC)

, resulting in CaCObetween two electrodes immersed in saltwater

3 and magnesium hydroxide

Mg(OH) deposition on the cathode. Depending on the induced current, the ratio between the 2

(Brucite) will be shifted. Less current tends (Aragonite) and Mg(OH)crystalline form of CaCO23

This substrate shows similarities Aragonite (Hilbertz 1992). to result in the more stable form

to naturally occurring reef limestone, and is therefore a good settlement substrate (van reeck T

ransplanted corals are cemented with the ongoing accretion into this Tand Schuhmacher 1997).

The chemical reaction of material, making additional fixation unnecessary (Eisinger 2005).

the electrolysis leads to an increase in pH-value and with that to an enhancement of mineral

precipitation around the cathode from supersaturated medium (Hilbertz and Goreau 1996). Both

are believed to support and facilitate access for the physiological processes of calcification and

coral growth (reviewed in Sabater and ap 2004). Goreau et al. (2004) also measured higher Y

densities of zooxanthellae in some species, but lower chlorophyll concentrations per symbiont cell

in coral transplants. Both coincided with higher coral skeletal growth rates and better developed

, which are seen as indicators of health in coral. In contrast, Sabater and branching morphology

Porites cylindrica ap (2002) measured a significant increase in girth growth in the basal region of Y

nubbins, but no increased linear growth.

The mineral accretion method still has not been tested adequately as most of the previous studies are

ap (2002), which is the only paper known Ylacking real controls with the exception of Sabater and

to the author using an experimental set up with a control. Many factors are still undetermined

with regards to this method such as applicable species, ideal fragment size, structure design,

67

Also the observations of enhanced coral location for deployment and amount of electrical current.

growth remain subjective as no comparison with growth data from donor colonies were made

in previous studies. It also remains unclear from the inventor side, if the attached corals have s’

to be in direct contact with the cathode, or if exposure to the electrical field already stimulates

The present work addresses these open questions as it sets a positive transplant performance.

out to test the hypothesis that increased growth and higher survival rates are due to stimulation

from an electrical field in direct comparison to those without electrical stimulation and branches

within the donor colonies. Further it will clarify whether a positive response by fragments varies

among the transplanted species and whether the design of the electrified structure has a significant

impact. It also addresses differences in survival, density of zooxanthellae and their chlorophyll

concentration in the presence and absence of the applied electrical current.

Methods

ransplant response of T

opora yongeiAcrA. pulchra and

ferent experiments. was tested in three dif

f Lihage Island (1º45’36”N, Fragments were taken from a shallow reef terrace in 4 m depth of

125º02’16”E; Fig. 1), in July 2005 for the 1

Fig. 1

Island.

st experiment and in March 2006 for the 2

Manado

Lihage

Gangga

N

m10k

nd and 3

rd

Map of North Sulawesi, showing the sampling site on Lihage and the experimental site on Gangga

68

experiments. All coral fragments of both species originated from an extensive, mixed coral stand

-sized fragments (6-8 . Fingerapproximately 30 m long and 15 m wide with 95 % live coral cover

, which sometimes had two axial polyps - were A. pulchracm), generally with single tips – except for

They were then transported f using a long-handled pliers to minimize tissue necroses. broken of

in buckets with seawater within 10 minutes to Gangga Island (1º45’35”N, 125º03’15”E; Fig. 1)

The attachment of transplants was and placed in baskets next to the transplantation structures.

, depending on the experiment. Each conducted within 24 hours with plastic cable ties or epoxy

ferent approach:experiment focused on a dif

Experiment 1: testing the effects of differ

transplants

owth of coral ents on the grent electrical curr

Three tunnel shaped structures (6 m length, 1.5 m height, 2 m width) were welded from construction

rebar (ø 12 mm) and uncoated, standard chicken wire to form the transplantation base (Fig. 2

2They were anchored at a depth . a). Each tunnel structure had a metallic surface area of 4.2 m

2An anode (1.5 m. of 5-6 m on the sea floor 4 m apart from each other titanium mesh; 39.4

mesh m-1; approximately 0.025 m2 of surface area m-2 of mesh (data from A. Spenhoff personal

communication) was deployed under the transplantation tables of each of the electrical loaded

The four electrodes, two cathodes and two anodes, were structures (from here on “cathode”).

connected with separate 130 m-long copper cables (each with three inner wires of cross-sectional

area 2.5 mm2 each) to two land based common automobile 12 V-battery chargers (Delta-brand

Ah). Separate cables for each pole were used in order to minimize electrical resistance due to 60

The connection points between the cables and small diameter and length of conductor material.

, to avoid any corrosion. Epoxy coverings are critical due the anodes were isolated with epoxy

low-current electrical field was Ato the acidic pH-environment generated around the anodes.

(theoretical Agers were set to 7 then induced between the cathode and the anode. Battery char

calculated current density of ~1.67 A m-2 cathodic surface) for one structure and 10 A (~2.38 A m-2

ferences of fragment growth rates caused cathodic surface) for the second to test for possible dif

by the strength of the electrical field.

-break gers were running continuously during the entire experiment time, with a daily 2-hour Char

measurement of the electrical AThe third structure was used as a control. to avoid overheating.

output and ph-value around the electrodes was not possible and therefore a visual inspection of

. gers was used as an indicatormineral accretion and output as displayed by the battery char

species were lodged into the chicken oporaAcrOne hundred fifty fragments of each of the two

mesh of the structures 1.4 m above the reef substrate. In the case of the control structure, fragments

were secured with plastic cable ties.

69

Fig. 2

From top to bottom a) experiment 1:

unnel structure with chicken wire transplantation table. T

An anode was placed on the ground under the transplantation table b) experiment 2:

ransplantation T

tables with different height levels, the anode is located in the middle of the triangle, note: photo shows

structure before start of actual fragment transplantation, c) experiment 3: Matrix frame with alternating

metal (cathode) and bamboo boards (electrical field). Notice that fragments were glued into concrete cups,

and 25 opora yongeiAcrwhich were then strapped on the bamboo boards. Each of the boards is holding 25

fragments. Horizontally placed anodes were deployed on each side of the matrix as seen in the A. pulchra

front of the photo.

70

ee Experiment 2: testing the effects of transplantation height on fragment performance with thr

elevation levels

ferent levels of elevation (one slightly above wo sets of three transplantation tables, with difT

the sediment, one raised 0.8 m and one 1.6 m above the sediment), were welded from rebar and

ferent elevations were chosen in order connected to each other in a triangular form (Fig. 2b). Dif

to test the effects height has on performance. Each table set had a surface area of 3.5 m2. A 0.36

2 mitanium mesh anode was wrapped around a PVC-pipe and vertically fixed in the triangle T

130 m long copper cable was connected to the anode while Acenter formed by the three tables.

a second was split 3 m before the table-set and connected to each table at identical point. Cables

The second, ger as described in experiment 1. Ah battery charwere connected to a Delta-brand 60

unconnected set was used as a control. These arrangements were deployed at a depth of 7 m at a

.distance of 6 meters from each other

species was attached to both the cathode oporaAcr total of 54 fragments from each of the two A

charged with 12 A (~3.43 A m-2 cathodic surface) and to the control. Equal fragment numbers were

gers was the same The daily operational time of the charused for each of the three height levels.

as in the previous experiment.

AExperiment 3: ent attachment methods comparison of differ

. It consisted of five matrix with the dimensions of 5 m x 2 m was welded from ø 0.87 cm rebarA

2 grid fields alternated with five open fields (Fig. 2c). 1 m

Small steel tubes (length 4 cm, ø 2 cm) were welded onto each grid stack as transplantation

2The matrix (“cathode” from here on), with a metal surface area of 4.2 msockets. , was deployed at

2 and 2 x 0.45 a depth of 4 m on a protected sandy bottom. Four titanium mesh pieces (2 x 0.30 m

2, on each , “anode” from here on) were wrapped around PVC pipes and installed horizontallym

side, at a distance of 50 cm from the cathode. One 120 m copper cable connected two sides of the

matrix with a 12 ger while a second 120 m copper cable connected the four anodes -battery charV

The cables The multiple connection points guaranteed an even current distribution. . gerto the char

Ager set to 12 were isolated as described in the previous experiments and the battery char (~2.86

-2 cathodic surface) with a daily 2-hour operational break to avoid overheating. A m

Bamboo grid boards were laid into each of the five open fields (from here on “electrical field”).

Four additional bamboo boards, for control fragments, were laid out at a distance of 4 m from

total of 700 coral fragments were assigned to the three Athe matrix (from here on “control”).

The first consisted of coral fragments lodged into the metal tubes with direct contact treatments.

The second treatment consisted of coral ged metal (= cathode, each species n = 125). to the char

fragments cemented into concrete cups, strapped onto the bamboo boards and exposed to the

71

electrical field (= electrical field, each species n = 125). In the third treatment the coral fragments

were placed in concrete cups, on bamboo boards, outside the electric field (= control, each species

n = 100).

owth measurGrement

Linear growth of fragments was measured with calipers at six-week intervals over a period of eight

months. Either the lock of an attached cable tie or the Epoxy base was used as the measurement

The number of surviving fragments was counted on every frame in each six-week reference point.

interval. If fragments with broken tips were recognized during measurement, these fragments

were not counted for this measurement period.

Simultaneous growth data from branches within the donor colonies were collected to compare

ferent colored cable ties were used as natural growth with growth of manipulated fragments: dif

markers and reference points for the measurement.

period of up to 10 months.

The experiments were examined during a

ophyll concentrationeatment for zooxanthellae count and chlorrT

After three months, coral samples were collected from each table of experiment 2 and the donor

colonies to measure the density of zooxanthellae and chlorophyll-a and -c concentrations. Samples

were packed into dark plastic bags, immediately frozen after collection and stored in an icebox

Tuntil further procedure. issue of each sample was removed with an airbrush gun and seawater

issue parts were finely ground and the blend was filled up to 40 ml with seawaterTin half-light.

Samples of 5 ml were removed from this solution, and preserved with 1 ml Formalin (40%)

.

The remaining solution was re-frozen for later chlorophyll analysis. for the zooxanthellae count.

Zooxanthellae from the sub samples were counted in a Neubauer Counting chamber

standard procedures.

For surface estimations, the blank skeletal fragments were coated in

, following

arnish, to close all pores, V

weighted, recoated in paraffin and then weighted a final time, utilizing the technique of Stimson

This technique was repeated on objects with a known surface area to establish and Kinzie (1991).

s surface area was The coral’a calibrating diagram with weight and surface area as diagram axis.

then calculated using the resulting regression line of the diagram. From each of the preserved

sample solutions, chlorophyll was extracted from sub-samples, as described in Gardella and

Edmunds (1999), and measured in a Spectrophotometer for chlorophyll a and c concentrations.

72

Data analysis

All of the data were checked with the Grubbs Outlier test (Grubbs 1969) and were excluded fect of treatment on average growth was analyzed for each species, using The ef. when necessary for Experiment 2 (factor 1: A for Experiment 1 and 3, and a two-way-ANOVAa one-way-ANOVtreatment, with two levels; factor 2: transplantation height, with three levels) at 5% significance ukey-Kramer HSD test was conducted at 5% significance level, to reveal the T post-hoc Alevel. All growth data was transformed with log (ln) transformation, ference. location of significance difAlthough, in est for variance homogeneity (Glass 1966). Tthe data was then tested with the Levene is usually AANOV, an some cases a Levene test showed a small deviation from homoscedasticityrobust to small departures (Underwood 1997). This was also supported by a Welch-ANOVA test,
A. ANOVproving equality of group means and allowing the further use of the

able 1TOverall survival and loss of fragments at the end of the experiment time, given in percent. Survival was calculated after the observation of lost fragments.

treatment

10AExp1

7A

control

A. yongei A. pulchra

n

106

105

50

35 A) cathode high (12 Exp 2

25 A) cathode middle (12

26 A) cathode low (12

control high

control middle

control low

A) cathode (12 Exp 3

electrical field

control

20

20

21

250

250

100

survival loss n

1% 98%

0% 98%

12% 96%

86% 0%

0% 76%

0% 54%

0% 80%

0% 95%

19% 0%

0% 57%

0% 93%

0% 78%

22

23

10

21

25

26

20

20

22

250

250

100

survival loss

0% 95%

0%100%

0%100%

0% 91%

92% 0%

0% 42%

0% 90%

0% 90%

0% 91%

0% 52%

82% 0%

0% 47%

73

s illiam’Wfects of treatment on transplant survival were tested using a likelihood (G) test with The ef (SAS Institute Inc., USA) and KaleidaGraph (SynerAll data was analysed using JMPcorrection. gy Software, USA). Growth data from the donor colonies (n = 10) were excluded from statistical analysis, as numbers , displayed in the They were, however. of replicates in the experiments were a 5 to 12 fold highergraphs.

Results

etion rates on the cathode structurObservation on the anodes and of accres

ged with comparable high ampere values can result in gas It is noted that small anodes charevolution and an acidic plume around the anode, but such observations could not be made for any fect of acidic plumes on dissolving arogonite deposition or on The possible efof the experiments. coral growth remains unaccounted. treatment and AAccretion in experiment 1 after 9 months ranged from 4 to 24.5 mm on the 10 The smaller values were measured towards the sides of the treatment. from 2 to 18 mm on the 7AAccretion around the centered chcken wire transplantation platforms ranged from 20 structures. to 24.5 mm. In experiment 2 the accretion ranged from 2 to 18 mm on the low table as a result of contact with the sandy bottom, 22 to 37 mm on the middle table and 16 to 34 mm on the high A. In experiment 3 the mineral accretion on the matrix ranged table, after 9 months treated with 12 A. Due to the slow accretion rate and its hard from 12 to 24 mm after 7 months treated with 12

Table 2 Two-way ANOVA of average monthly length increase of Acropora yongei and A. pulchra in
Experiment 2 after 8 month of exposure to 2 treatments (factor 1: treatment, with two levels): 1) direct ferent ged metal frames of same design) on 3 difcontact with the cathode, 2) control (mounted on unchar.elevation levels (factor 2: transplantation height, with three levels): 1) high, 2) middle, 3) low

A. yongei

A. yongei Source df MS
/

545 473 otal T

F p A. pulchra

dfpF MS

Treatment 1 2.904 35.326 < 0.001 1 210.22 33.469 < 0.001

Height 2 0.088 1.071 0.344 2 61.399 9.776 < 0.001

Interaction 2 0.271 3.297 0.038 2 37.509 5.972 0.027

74

Aragonite rather appearance it is most likely that the mineralization that occurred produced hard than soft Brucite.

owthents on coral grent electrical currExperiment 1: the influences of differ

steadily increased their monthly growth rates over time in all A. yongeiransplanted fragments of T showed only an increase within the first three months of A. pulchratreatments (Fig. 3.a), while The average monthly transplantation, before reaching a steady state of average growth (Fig. 3b).

a)121110987average growth [mm/ month]6543210Aug-2005b)121110987average growth [mm/ month]6543210Aug-2005

Oct-2005Oct-2005Dec-2005Dec-2005Feb-2006Feb-2006Apr-2006Apr-2006Jun-200610A7Acontrol

Jun-2006Fig. 3 Average monthly growth changes (± SD) over time for a) Acropora yongei (n = 266) and b) A.
A. pulchraferent electrical currents. Notice that controls for (n = 55) on structures powered with difpulchrahave been measured only during the last three periods. 75

a)

b)

average growth [mm/ month]

average growth [mm/ month]

9

876543

2

10

9

876543

2

10

A

10A

AA

10A

B

7A

B

7A

B

control

control

donor colony

donor colony

Fig. 4 Comparison of average monthly growth (± SD) for a) Acropora yongei and b) A. pulchra fragments
ferent electrical currents in Experiment 1 and growth rates in donor colonies (n = 10). treated with difNotice that the control in b) only displays data for three month. Letters in a) indicate results of a post hoc Tukey-Kramer HSD test. Letters in b) indicate significantly differences after a ANOVA testing only 10A
ferences.ferent letters indicate significantly difand 7A. Dif

76

treatment with 6.5 mm Alength increase of electrical treated transplants was the highest on the 7 ± 0.6 (mean ± SD) for A. yongeiThere was a correlation between growth and strength of an electrical current for transplanted (Fig. 4a) and 5 mm ± 0.7 (mean ± SD) for A. pulchra (Fig. 4b).A.
yongei (ANOVA, p < 0.001, df = 2, F = 11.54). A. yongei showed significantly lower growth rates
in treatment 10 A than in treatment 7 A or the control (Fig. 4a). Similarly, the growth rates of A.
pulchra in the 10 A treatment were significantly lower than in the 7 A (T-test, p < 0.001, df = 1, F
= 25.05; Fig. 4b). A. yongeiable 1). In both electric treatments, Survival of fragments in all treatments was high (T A. pulchrashowed a mortality of only 2 %, while transplants on the control had a mortality of 4 %. structure. A and control structure, but a 5% mortality on the 10 Ashowed 0 % mortality on the 7 A. Loss of fragments due to physical impacts could be noticed only on the control structure for (12%).pulchra

owth, zooxanthellae ent height levels on grExperiment 2: the effects of transplantation at differophyllnumber and chlor

able 2). The correlation between height levels and treatments for both species was significant (T transplants during the 8-month period reached A. yongeiThe average monthly growth rates for -1 ± 0.3 (mean ± SD) on the high control level (Fig. 5.a), although a maximum of 3.3 mm month significantly higher Aference between heights for any treatment. there was no significantly difable 2; Fig. 5b). Growth compared to the treated (TA. pulchragrowth was measured for control 4.7 mm monthalso significantly dif-1fered between heights for ± 0.2 (mean ± SD) on the middle control level (TA. pulchraable 2; Fig. 5b). transplants with the highest average of
ference in The zooxanthellae count, recorded three months after fragmentation, showed no different height treatments for the two species. zooxanthellae abundance when comparing the dif did show a significant higher cell density on the cathode compared to the A. yongei, Howevercontrols (Table 3a; Fig. 6a). Therefore cell number in A. yongei branches in the donor colony
(6.447*105 cells cm-2 ± 3.924*105; mean ± SD) was almost twice as large as in fragments on the
cathode (cathode middle; 3.362*105 cells cm-2 ± 1.525*105; mean ± SD). There was no significant
able 3a; Fig. 7a).(TA. pulchra ference in cell density in dif testing the height and the interaction between height and treatment showed AThe two-way-ANOVable 3b, fect on chlorophyll-a concentrations in zooxanthellae for both species (Tno significant ef, zooxanthellae had significant higher concentrations of chlorophyll-a in Fig. 6b & 7b). Howeverable 3b, Fig. 6b & 7b). Height and treatment showed fragments of both species on the cathodes (Ta significantly effect on chlorophyll-c in A. yongei (Table 3c; Fig. 6c) but not in A. pulchra (Table
3c; Fig. 7c).able 1) was the lowest on the middle position of the control structure Mortality of fragments (T

77

a)

b)

average growth [mm/ month]

average growth [mm/ month]

9

876543

2

1

0

9

876543

2

1

0

A

high

a

high

B

middle

a

middle

low

bA

low

donor colony

cathodecontroldonor colony

donor colony

Fig. 5 Comparison of average monthly growth rates (± SD) for a) Acropora yongei and b) A. pulchra
ferent heights in Experiment 2 and growth rates in donor colonies (n = 10). Letters in b) fragments on differences.ferent letters indicate significantly difukey-Kramer HSD test. DifTindicate results of a post hoc

(5 %) for A. yongeihighest mortality rate (81 %). A. pulchra. Fragments transplanted in the low position on the control structure had the transplanted on the low cathode had a mortality rate
ference in survival rates when compared to the other of 58 % but did not show a significant dif comparison between fragments transplanted on the cathode and the control structure Apositions.

78

b)22201816chlorophyll a [μg/10+e6 cells]

cathodecontroldonor colony

a)7 105b)22c)22cathode
control20donor colony2056 10181816A5165 10A1414a54 101212zooxanthellae [cells/cm]chlorophyll c [μg/ 10+e6 cells]1010chlorophyll a [μg/10+e6 cells]53 10B8b852 1066b4451 10220highmiddlelowdonator colony0highmiddlelowdonor colony0highmiddlelowdonor colony

Fig. 6 Comparison of a) zooxanthellae densities (cells cm-1), b) chlorophyll-a (g 106 cells-1) and c)
chlorophyll-c (g 106 cells-1) for Acropora yongei (n = 6) in different transplantation heights after 4 months
HSD test. Different letters indicate significantly difin experiment 2. Error bars indicate standard deviation. Letters indicate results of a post hoc ferences.Tukey-Kramer

on the control structure (Likelihood A. pulchrashowed a significantly higher survival rate for test with William’s correction: p < 0.001), while A. yongei showed no difference. A significant
ference occurred in mortality for the low positions between the two treatments (Likelihood test: difp < 0.01), with higher survival rates for A. yongei on the cathode and A. pulchra on the control.
owthent attachment methods on grExperiment 3: a comparison of the effects of differ

The treatment had an efinside the electrical field (4.8 mm month-1 fect on both species after 10 months: A. yongei± 0.3; mean ± SD), than on the control (3.3 mm month grew significantly faster -1

cathodecontroldonor colony

a)8 105b)22c)22
cathodecontrol20205donor colony7 10181856 101616145145 10chlorophyll a in [μg/10+e6 cells]zooxanthellae [cells/cm]1212chlorophyll c [μg/10+e6 cells]54 10101053 10886652 104451 10220highmiddlelowdonator colony0highmiddlelowdonor colony0highmiddlelowdonor colony

Fig. 7 Comparison of a) zooxanthellae densities (cells cm-1), b) chlorophyll-a (g 106 cells-1) and c)
chlorophyll-c (g 106 cells-1) for Acropora pulchra (n = 6) in different transplantation heights after 4 months
in experiment 2. Error bars indicate standard deviation.

79

Table 3 Two-way ANOVA for a) zooxanthellae densities, b) chlorophyll a and c) chlorophyll c
concentrations of zooxanthellae in experiment 2 after 4 months of exposure in Acropora yongei and A.
ferent to 2 treatments (factor 1: treatment, with two levels): 1) cathode, 2) control and on 3 difpulchra.elevation levels (factor 2: transplantation height, with three levels): 1) high, 2) middle, 3) low

pulchraA. yongei A.

Source df MS F p MS F p
-2)a) zooxanthellae density (cells cm

35 total 10 1.997*10 1 treatment height 2 3.324*109
10 2 interaction 6.458*1010 2.778*1030 error

-16 ) cellsb) chlorophyll-a (g 10

35 total 303.805 1 treatment 2 height 67.556 49.324 2 interaction 30.928 30 error

c) chlorophyll-c (g 106 cells-1)
35 total 95.583 1 treatment 2 height 149.502 28.350 2 interaction 6.689 30 error

35 7.089 0.012 1 1.813*1010 2.12 0.156
1.196 0.316 2 7.149*109 0.84 0.443
2.325 0.115 2 1.980*1010 2.31 0.116
30 8.560*109

35 0.00310.75 1 149.572 0.004 9.82 0.3581.06 2 14.796 0.130 1.18 0.3671.04 2 14.421 0.220 1.59 30 13.908

35 0.0873.13 0.004 1 31.323 9.86 0.1691.89 < 0.001 2 18.865 15.42 0.4760.76 0.069 2 7.598 2.926 30 9.993

-1 ± 0.3; mean ± SD) (T± 0.3; mean ± SD), or in direct contact with the cathode (2.5 mm monthable showed a decreasing trend of growth over time in the electrical field A.yongei, 4; Fig. 8a). Furtherand control boards, while fragments on the cathode showed a improving trend of growth (Fig. 9a).

transplants in this experiment grow significantly better in the electrical field treatment A. pulchra

80

(2.3 mm month-1 -1 ± 0.2; mean ± SD) and on the cathode (2.1 mm month-1 ± 0.2; mean ± SD) than
The average growth rates able 4; Fig. 8b). ± 0.2; mean ± SD) (Ton the control (0.9 mm monthdecreased in all treatments over time for this species (Fig. 9b).

Branches in the donor colonies of both species grew faster than those of the transplanted fragments A. pulchraference in in the experiment. Dif was most obvious with branches in the donor growing four times faster than transplants.

fragments showed a significant higher mortality A. yongeiowards the end of the experiment 3, Tof 43 % on the cathode compared to the transplants of the control and in the elctrical field where

a)

average growth [mm/ month]average growth [mm/ month]

b)

average growth [mm/ month]

9

8

7

6543

2

1

09

8

7

6

5

43

2

1

0

A

cathode

A

cathode

B

electrical field

A

electrical field

C

control

B

control

donor colony

donor colony

Fig. 8 Average monthly growth changes (± SE) over time for a) Acropora yongei and b) A. pulchra
in direct contact to the cathode, inside an electrical field and on control boards in experiment 3. Letters ferences.ferent letters indicate significantly difukey-Kramer HSD test. DifTindicate results of a post hoc

81

Table 4 ANOVA of average monthly growth increase for Acropora yongei and A. pulchra in experiment
3 after 10 months of exposure to 3 treatments: 1) direct contact with the cathode, 2) inside the electrical field, 3) control.

Source of variation

1total treatment 1error

A. A. yongei

pulchra

df MS F p df MS F p

743 151 2.284 38.132 < 0.001 2 61.289 < 0.001 5.594 2 741 0.091 149 0.06c

mortality was less than 25 % (Table 1; Table 5). Mortality of A. pulchra was significantly higher
able 1; on both, the cathode (48 %) and the control boards (53 %) than in the electrical field (Table 5).T

A. pulchra branches in the donor coloniesopora yongei and AcrObservations on

The average monthly length increase of branches within the donor colonies was 5.6 mm ± 0.2 (n = 10) A. pulchra (n = 10) (Fig. 5a) and 8 mm ± 0.5 (mean ± SD) for A. yongei(mean ± SD) for (Fig 5b). Zooxanthellae density in A. yongei was 6.45*105 cells cm-2 ± 9.612*104 (mean ± SD)

Table 5 Likelihood (G) tests with William’s correction comparing mortality rates of Acropora yongei and
after 10 months grown on a cathode, inside an electrical field and control.A. pulchra

GComparison

A. yongei
p df adj

< 0.001 1 32.12 cathode x electrical field cathode x control < 0.001 1 17.53 0.07 1 3.37 electrical field x control

A. pulchra df p Gadj

< 0.001 1 22.05 0.67 1 0.18 < 0.001 1 20.81

82

a)7654average growth [mm/ month}3210May-2006

b)7654average growth [mm/ month}3210

May-2006

Jun-2006

Jun-2006

Jul-2006

Jul-2006

Aug-2006

Aug-2006

Sep-2006

Sep-2006Oct-2006

Oct-2006Nov-2006

Nov-2006Feb-2007Dec-2006

cathodeelectrical fieldcontrol

Dec-2006Feb-2007Fig. 9 Comparison of average monthly growth (± SE) for treated a) Acropora yongei and b) A. pulchra
ukey-Tfragments of experiment 3 with growth rates in donor colonies. Letters indicate results of a post hoc ferences.ferent letters indicate significantly difKramer HSD test. Dif

-16 ± 0.49 (mean ± SD) and chlorophyll-c cellswith a chlorophyll-a concentration of 10.435 g 10concentration of 5.548 g 106 cells-1 ± 0.646 (mean ± SD) (Fig. 6). Zooxanthellae density in A.
pulchra was 4.34*105 cells cm-2 ± 6.523*105 (mean ± SD) with a chlorophyll-a concentrations of
12.265 g 106 cells-1 ± 1.207 (mean ± SD) but chlorophyll-c of 4.67 g 106 cells-1 ± 0.302 (mean
± SD) (Fig. 7).

83

Discussion

oporaAcrwo species of T

fragments, testing the effects of electrical current on growth rates and ferences in three coral transplantation experiments.survival, demonstrated significant dif

Coral transplantation is a preferred method in rehabilitation and restoration projects, but the

quality of such a technique is not always assured (Edwards and Clark 1998). Although it leads

to an immediate coral cover and attraction of reef inhabitants (see Ferse 2008), this technique

can only be considered positive if the long term performance of fragments is positive (Clark and

Edwards 1995).

The critical point, Consequently the first concern applies to the survival of coral transplants.

The present study focused on the therefore, is the size in accordance to the attachment method.

oporaAcruse of branching

fragments, as members of this family are known to exhibit good growth and survival rates if conditions are favorable (reviewed in Knowlton and Jackson 2001).

oporaAcrThe identically sized

fragments of approximately 8 cm length collected from the same . In the first step these fragments were loosely donor allowed a direct comparison with each other

attached to the electrical structures (cathodes), but gained a firm attachment through the ongoing

mineral accretion within a matter of days. Loss of less than 1% of the fragments on the cathodes

clearly proved a secure attachment with the mineral accretion method. pulchra

A. and Acorpora yongei

survival rates of more than 75 % for both species coincided with findings of Schuhmacher ap (2002) who tested the mineral accretion technique for other coral Yet al (2000) and Sabater and

Bowden-Kerby (1997), who seeded unfixed branching coral fragments on sandy bottom, species.

-sized fragments and was just able to increase fragment survival counted 100 % mortality for finger

Also Smith and Hughes (1999) recorded when using a relatively big initial size of more than 30 cm.

ferent reef substrate a low overall survival of seeded coral fragments, although they monitored dif

environments. In both cases sedimentation was one of the major factors for low survival rates. On

-sized fragments of Okubo et al. (2005), firmly attached to concrete nails the other hand, finger

and driven into the substrate, reached survival rates of up to 100 %. Firmly attached fragments on

the controls showed similar high survival patterns in the present work, but such firm attachment

was more time and material consuming than fast and easy attachment to cathode structures. Other

factors than the attachment method were more likely to be responsible for disappointingly low

. survival in some experimental treatments, as discussed below

While high survival rates have been demonstrated by multiple other transplantation techniques,

ap and Gomez 1985, Ythey often also showed a reduced growth rate amongst fragments (see e.g.

YCustodio III and fects of stresses from handling, This may be partly due to lasting efap 1997).

transport and transplantation technique or unsuitable transplantation sites.

ferences between the experiments, but these The present study was able to demonstrate growth dif

experiments were not able to demonstrate the enhanced coral growth rates several times greater

than normal as reported by the inventors of the method (see Hilbertz and Goreau 1996, Goreau et

84

al. 2004, Goreau and Hilbertz 2005). The fragments that were exposed to the weakest currents on

-2), those in the electrical field and those in the control group showed the best mAcathodes (< 1.7

growth rates - comparable with those of the natural colonies.

The electro-chemical process of mineral accretion is a result of a pH-increase from a shift of

ganic carbon), concentration gradients of dissolved minerals, as for example DIC (dissolved inor

near the cathode. Coral growth on the other hand involves the uptake of DIC to build the CaCO 3

skeletons. Controlled studies in aquaria proved, that corals kept in DIC-enriched seawater enhance

Thake 1999). Hence it is believed that this extra concentration of DIC their growth (Marubini and

is available for corals transplanted on the cathodes and so enhances transplant growth. Sabater and

ap (2002) suggested the idea that these mineral ions are concentrated a few millimeters above Y

fected than vertical growing ones the cathode so that laterally growing species should be more af

which were used in present studyThis hypothesis is based on their findings of extended girth .

growth and supported by the results of Schuhmacher et al (2000), who measured increased foothold

, the present study showed decreased growth rates with in vertically growing species. However

electric current outputs set to 10 and 12 A (respectively more than 1.7 A m-2) or when coral tissue

As higher amperage yields a higher alkaline environment was in direct contact with the cathode.

around the cathode, indicated by precipitation of settlement-inhibiting Brucite (Eisinger et al.

Accretion thickness fects of a higher DIC concentration. 2005), it might outweight the positive ef

Thin accretion areas were often localised to areas where often varied greatly within the structures.

, the rebars were welded together or where the material was deformed. Changes in the conductivity

resulting in an uneven electrical field and varying accretion thickness can be caused by poor

quality welding points and material deformation. Hence, variation of average growth rates of

fected by the local thickness of the accretion coatings, which was an fragments may have been af

direct correlation between variations of Aunmonitored aspect of the electro-chemical processes.

. accretion and coral growth remains unclear

ap (2002, 2004) and Eisinger (2005) noticed enhanced growth rates only YWhile Sabater and

during the early stages of mineral accretion, present results demonstrated a variation in growth

rates linked to the amperage: coral growth increased over time when amperage was low (Fig. 3)

, the total average but demonstrated a decreadsing rate, when amperage was high (Fig. 9) . However

growth rates remained in almost every experiment lower than those of the donors (Fig. 4b, Fig.

ransplantation stress cannot be ruled out and could have caused the lower growth T5 & Fig. 8).

An additional explanation rates in the beginning of the experiments (Clark and Edwards 1995).

ith Wis the morph of fragments used, as they were all comparably short with single growth tips.

ongoing time and extension of the fragments, the number of growth tips increases. Rinkevich

(2000) demonstrated that fragments with multiple growth tips reached twice the total length of

the single-tip fragments in the same amount of time, which might be due to nutrient circulation

and ener2000).

gy transfer within the underlying tissue which supports Acreron apical growth (Vopora

85

ap and Molina (2003) found that transplantation of fragments of species that were both closely Y

ferent responses to their new transplanted sites, related and dominant in the same reef area had dif

Tdespite very similar environmental conditions. ransplants ofin present A. yongei and pulchra A.

The strong discrepancy of growth between transplants . study demonstrated a similar behavior

regardless of treatment and donor colony as seen in Fig. 4, 5 and 9, demonstrates that is the species more sensitive to transplantation.

showed no difA. pulchraThe number of zooxanthellae in

A. yongei. the donor

A. pulchra

ference between the treatments and transplants demonstrated significantly higher cell numbers than those in the . Chlorophyll-control, although they were only half the cell number as counted in the donor colony

a concentrations in transplats on the cathodes were significantly higher for both species, than

These measurements coincided with lower growth rates for the those of the controls and donors.

ferent cathodes. Goreau (2004), who conducted alike measurements on dif species, found oporaAcr

no significantly dif, but lower concentrations of chlorophyll-a coinciding ference in cell number

Three explanations for higher chlorophyll-a with higher growth rates in stimulated fragments.

concentration versus lower zooxanthellae number were reviewed in Jones (1997a):

, through decreased competition of zooxanthellae, b) breakdown a) an increased nutrient availability

products of chlorophyll interfere with absorption peaks during measurement, c) greater loss of

zooxanthellae from the apical tissue, leaving dark-adapted behind.

It remains unclear whether the higher chlorophyll concentration is due to one or a combination of

the above factors, or an interaction between these factors and the electrical field. If a reduction in

zooxanthellae density is an indicator of physiological stress (Jones 1997b) the above results would

imply that transplants are more stressed than donors and treated fragments are more stressed than

untreated.

rdnd experiments with their low survival and growth rates, the following and 3In retrospect of the 2

nd experiment were exposed in the things should be mentioned: Fragments on the cathodes in the 2

beginning of the experiment to increased predation by coralivorous fishes and numerous dislodged

Although pieces of fragments were found spread out around the structure (personal observation).

it was only noticed during the first two months of the experiment - and damaged fragments were

exchanged and not counted during that measure period – a subsequent but unnoticed fish predation

leading do a decreased growth could not be ruled out, as growth measurements were conducted in

The transplantation technique used for the . 6-weeks-intervalls, giving tissue enough time to recover

rdcontrol boards in the 3 experiment demonstrated in a neighboring transplantation project 100 m

apart from the electrical structure, impressively high growth rates for the same species located in a

Therefore the placement of boards between two extensive identical depth (personal observation).

Euphyllia ancora

colonies (10 x 10 x 3 m) must be considered as a possible explanation for the E. ancorapoor performance.

is described as a very aggressive coral, protecting its space with , as there was no direct contact between sweeper tentacles (Lewbart and Lewbart 2006). However

, a secretion of some unknown repellents analogue to terpenoid compounds, E. ancoracontrols and

86

as used by soft corals (Maida et al. 1995), could have added to the poor performance. Fragments

nd experiment on the low ground level tables were more exposed to sedimentation and in the 2

sedimentation is known as a stress factor causing decreased coral growth rates (Cruz-Pinon et al.

2003, Crabbe and Smith 2005).

Conclusion

The flexibility in design allows a The mineral accretion technique has obvious advantages.

. customized approach for many purposes. Its ease of installation tolerates limited manpower

Coral transplants are easy to secure and attach with hold constantly improving with the increase

The extremely high survival rates of coral transplants as demonstrated of mineral accretion.

especially in experiment 1 are convincing for a successful transplantation project.

On the other hand it also has some critical points that have to be considered when planning the use

get species, as not all species of this technique: a) caution has to be taken when choosing the tar

-2 cathodic mAare receptive to electrical stimulation, b) an increased electrical current over ~1.67

surface does not seem suitable for maximum growth performance for the examined species,

c) direct contact to the cathode diminishes, rather than supports performance, d) bigger sized

fragments of branching corals with multiple growth tips seem to be better suited for transplantation

than fragments of branching corals with only a single growth tip as used here.

Acknowledgement

f from the Gangga Island Resort for all logistical I would like to thank G. Davi and his staf

Hilbertz and team for technical advice and .W, C. Shwaiko, support and the generous hospitality

fen, provided anode material, S. Ferse and S. Schmidt-Roach for their help in the field, J.-H. Stef

M. Schmidt, and A. Kunzmann for advices on the text and three anonymous reviewers for very

This work was supported by a DAAD PhD scholarship.helpful comments on the manuscript.

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Appendix

2

3

1

1

3

2

2

1

Cross section thru a Pocillopora verrucosa, 2 = ova with vacuuls and polyp. 1 = mesentery.pink coloured nucleus, 3 = spermary

Cross section thru Seriatr1 = polyp outline, 2 = egg, 3 = planula larvae.opora hystrix polyps.

branch opora yongeiAcrCross section thru an showing radial arranged egg (1) - sperm (2) - bundles.

92

93

Gemäß §6 der Promotionsordnung der Universität Bremen für die

- und ingenieurwissenschaftlichen Fachbereiche vom 14. mathematischen, natur

März 2007 versichere ich, dass:

Arbeit ohne unerlaubte fremde Hilfe angefertigt wurde 1. die

2. keine anderen als die angegebenen Quellen und Hilfsmittel benutzt wurden

erken wörtlich oder inhaltlich entnommenen Stellen als W3. die den benutzten

solche kenntlich gemacht wurden

Bremen, 24. September 2008

Sascha Romatzki

94