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Small-scale Differences in Tropical Subtidal Rocky Reef Communities of Floreana Island, Galápagos

Annika Krutwa

Doctoral thesis submitted in partial fulfillment of the requirements for the degree of Doctor of Natural Sciences (Dr. rer. nat.) to Faculty 2 (Biology and Chemistry), University of Bremen

Bremen, 30 July 2014

Charles Darwin Foundation

The present study was conducted at the Charles Darwin Foundation in Puerto Ayora, Galápagos (Ecuador) and compiled at the Leibniz Center for Tropical Marine Ecology (ZMT) GmbH (Germany).

This thesis was mainly funded by the German Academic Exchange Service (DAAD) through a research grant for doctoral candidates and the Charles Darwin Foundation. Additional financial support was provided by the ZMT and the German Federal Ministry of Education and Research (BMBF, Grant No. ECU 10/A01).

1. Reviewer: Prof. Dr. Matthias Wolff Leibniz Center for Tropical Marine Ecology (ZMT) GmbH 2. Reviewer: Prof. Dr. Kai Bischof University of Bremen

1. Examiner: Prof. Dr. Thomas Brey Alfred Wegener Institute for Polar and Marine Research (AWI) 2. Examiner: Dr. Claire Reymond Leibniz Center for Tropical Marine Ecology (ZMT) GmbH

Erklärung

Gemäß §6 der Promotionsordnung der Universität Bremen für die mathematischen, natur- und ingenieurwissenschaftlichen Fachbereiche vom 14. März 2007 erkläre ich, dass die Arbeit mit dem Titel:

“Small-scale differences in tropical subtidal rocky reef communities of Floreana Island, Galápagos”

1) ohne unerlaubte Hilfe selbstständig verfasst und geschrieben wurde;

2) keine anderen als die angegeben Quellen und Hilfsmittel benutzt wurden;

3) die den benutzten Werken wörtlich oder inhaltlich entnommenen Stellen als solche kenntlich gemacht wurden;

4) es sich bei den von mir abgegeben Arbeiten um 3 identische Exemplare handelt.

Bremen, ______Annika Krutwa

II

“...What impressionable youngster could resist the images of a mystical moonscape on earth, inhabited by giant tortoises large enough to ride, prehistoric iguanas that share a sea filled with fishes, sea lions and whales, and spreading above it all, a blue equatorial sky alive with the sailing silhouettes and sounds of ocean-going birds on the wing?..”

Paul Humann (1993) about Galápagos

Table of contents

List of Tables ...... III List of Figures ...... V Abstract ...... VII Zusammenfassung ...... IX Resumen ...... XI

Introduction ...... 1

Chapter 1: Pronounced small-scale differences between Galápagos subtidal rocky reef communities exposed to upwelling and non-upwelling conditions ...... 11 Abstract ...... 11 Introduction ...... 12 Materials and Methods ...... 14 Results ...... 17 Discussion ...... 21 Conclusion ...... 26 Acknowledgments ...... 27 References ...... 27 Appendix ...... 34

Chapter 2: Natural succession patterns on a tropical rocky reef (Galápagos, Ecuador) under upwelling and non-upwelling conditions ...... 41 Abstract ...... 41 Introduction ...... 42 Material and methods ...... 45 Results ...... 47 Discussion ...... 56 Conclusions and Outlook ...... 59 Acknowledgements ...... 60 References ...... 61 Appendix ...... 67

Chapter 3: Grazing effects on tropical rocky reef communities exposed to upwelling and non-upwelling conditions in Galápagos (Ecuador) ...... 69 Abstract ...... 69 Introduction ...... 70 Material and methods ...... 72 Results ...... 74 Discussion ...... 79 Conclusions ...... 82 Acknowledgements ...... 83 References ...... 83 Appendix ...... 89

I

Chapter 4: First insights into the food web structure of a tropical subtidal rocky reef community (Galápagos, Ecuador) using the stable isotope approach ...... 91 Abstract ...... 91 Introduction ...... 92 Material and Methods ...... 94 Results ...... 95 Discussion ...... 96 Conclusions ...... 101 Acknowledgements ...... 101 References ...... 101

Synthesis ...... 109

References ...... 121

Acknowledgements ...... 131

II

List of Tables

Chapter 1

Table 1. Water temperature statistics (in °C)...... 18 Table 2. Means of univariate measures of fish, mobile macroinvertebrate and fish community structure at LB and TC...... 19 Table 3. Results of PERMANOVA main test for macroinvertebrate and sessile community...... 20 Table A1. Species list...... 35 Table A2. Results of PERMANOVA main test for total cover of calcareous algae, encrusting algae, filamentous algae and macroalgae...... 39 Table A3. Results of PERMANOVA main test for total density of asteroids and echinoids...... 39 Table A4. Results of PERMANOVA main test for total fish biomass...... 39

Chapter 2

Table 1. Mean (±SD) percentage cover of taxa/species found on lava settlement plates on 7 different weeks during succession in La Botella and Tres Cuevitas (12-103 weeks)...... 48 Table 2. Analyses of similarity (ANOSIM) and similarity percentages (SIMPER) testing the effects of successional stages (in weeks) at each site and between sites for 12-, 30-, 54- and 103-week-old assemblages...... 54 Table 3. Overview of different analyses comparing univariate diversity measurements...... 55 Table A1. PERMANOVA tests on community structure on lava plates of two surface roughness types (S–smoothed, F–furrowed); LB=La Botella, TC=Tres Cuevitas...... 67

Chapter 3

Table 1. Analyses of similarity (ANOSIM) and similarity percentages (SIMPER) testing the effects of open vs. closed treatments at each site and between...... 78 Table 2. Results of fish and macroinvertebrate grazer surveys with list of counted herbivorous fishes and macroinvertebrate grazers and their proportion of the respective total count...... 79 Table A1. Species list ...... 89

III

Chapter 4

Table 1. Number of sampled replicates (n) for each species...... 94 Table 2. Comparison between estimated trophic levels by using the stable isotope approach (TLI) and the Ecosim with Ecopath approach (TLE)...... 96 Table A1. List of species registered during the study (2009-2011) in rocky reef habitat off Floreana Island...... 133

IV

List of Figures

Introduction

Figure 1. Map of the Galápagos Archipelago, with focus on Floreana Island...... 4 Figure 2. Schematic depiction of the major currents around the Galápagos Islands...... 5

Chapter 1

Figure 1. Study sites: Tres Cuevitas (TC) and La Botella (LB)...... 15 Figure 2. Temperature profile at TC and LB from March 2009 to March 2011...... 18 Figure 3. MDS ordination depicting relationship of monitored sites and surveys...... 20 Figure 4. Changes in percent cover, density and biomass (mean ± SE) of the main functional groups between seasons...... 21 Figure A1. Regression between monthly means of water temperature at 6 m and 15 m at study site TC (n = 22)...... 34

Chapter 2

Figure 1. A) Experimental lava substrates at 15 m depth at the non-upwelling site, Tres Cuevitas. B) Red algae Schizymenia ecuadoreana at the upwelling site (La Botella) C) Hard coral Pavona clavus at the non-upwelling site (TC)...... 46 Figure 2. Changes in cover of the most abundant functional groups (reaching > 5%) during succession at A) La Botella and B) Tres Cuevitas...... 51 Figure 3. Percent cover (±SE) of most abundant functional groups (reaching > 5%) surveyed in the adjacent area of succession experiments on March 2011 (successional stage: 103 weeks)...... 51 Figure 4. Non-metric multi-dimensional scaling (nMDS) plot showing differences in community structure between successional stages of different ages (12-103 weeks) and sites (LB=La Botella and TC=Tres Cuevitas)...... 52 Figure 5. Non-metric multi-dimensional scaling (nMDS) plot showing differences in community structure between the surrounding natural community and the 103 weeks old community and sites (LB=La Botella and TC=Tres Cuevitas)...... 53 Figure 6. Changes in average species richness (S) and evenness (J') during succession at both sites...... 55

Chapter 3

Figure 1. Study sites: Tres Cuevitas (TC) and La Botella (LB)...... 73 Figure 2. Non-metric multi dimensional scaling (nMDS) showing differences in community structure of different old epibiotic assemblages of open and closed treatments at LB and TC...... 75

V

Figure 3. Succession of various functional groups (>5% cover) in open and closed treatment at each site (LB and TC) over 103 weeks...... 76 Figure 4. Differences in species richness (S) and evenness (J’) of different epibiotic communities, LB and TC, exposed to open and closed treatments...... 77

Chapter 4

Figure1. Percentual (a) and stable isotope values (b) of carbon and nitrogen of sampled species...... 96

Synthesis

Figure 1. Interpolated temperatures to depth across 26 sampling stations spaced at 1 km intervals from west-north-eastern Floreana...... 112 Figure 2. Photos showing A) Coronaster marchenus B) Schizymenia ecuadoreana C) Gardineroseris planulata D) bleached Pocillopora sp. in front with Pavona clavus in the back...... 115

VI Abstract

Abstract

Tropical subtidal rocky reef communities are less prominent than coral reefs and characterized by macroalgae, mobile invertebrates, reef fish and diverse communities of epibenthic invertebrates. In the Galápagos Marine Reserve (GMR), more than 80 % of the shallow benthic habitats are rocky lava reefs, whereas coral reefs are the rarest habitat. Although surveys of the distribution and abundance of demersal fish, benthic invertebrates and algae are being conducted to gather baseline information for the GMR, sparse knowledge is available on small-scale variations in diversity, community structure and ecological processes under contrasting oceanographic conditions. In order to examine the effects of small-scale differences in oceanographic regimes, two rocky reef study sites (about 17 km apart), an upwelling and a non-upwelling site, were chosen off Floreana Island. The benthic community structure of the sites was studied for two years by subtidal monitoring including sessile organisms (algae and epifauna), mobile macroinvertebrates and reef fish. Simultaneously, benthic succession studies and grazer exclusion experiments were conducted at both study sites. Further, the food web structure for Floreana Island was analyzed by using the stable isotope approach. Results revealed significant differences between the sites regarding diversity and community structure, with the sessile community varying between seasons at the non-upwelling site. Moreover, succession patterns and grazing effects were distinct between sites. At the upwelling site a more predictable succession was obvious, whereas succession patterns were more random at the non-upwelling site. Grazer impact on community structure was weaker at the upwelling site despite significantly higher abundances of herbivorous fish and macroinvertebrate grazer than at the non-upwelling site, where strong grazing effects were evident. Hence, it was concluded that, depending on its oceanographic characteristics, the ecosystem is more bottom-up (upwelling site) or top- down (non-upwelling site) driven. Further, stable isotopes revealed that the food web of the rocky reef of Floreana Island consists of three trophic levels and results were compared with outputs of a trophic balanced model. Conclusively, these findings reflect the particular oceanographic setting of the Galápagos Archipelago and that Floreana Island may also represent a “model system” to investigate ecological responses along abiotic gradients. The occurrence of rare and threatened taxa together with introduced alien species in the studied rocky reef sites also shows that further investigations are

VII Abstract needed in order to apply adequate management strategies with the aim to conserve the uniqueness of the GMR ecosystems

VIII Zusammenfassung

Zusammenfassung

Lebensgemeinschaften tropischer sublitoraler Felsriffe sind unauffälliger als Korallenriffe und zeichnen sich durch Makroalgen, mobile Invertebraten, Rifffische und diverse epibenthische Invertebratengemeinschaften aus. Im Marinen Reservat Galápagos (GMR) sind mehr als 80 % der benthischen Flachwasserhabitate felsige Lavariffe, während Korallenriffe als Lebensraum selten sind. Obwohl Bestandsaufnahmen der Verbreitung und Abundanz von benthischen Fischen, Invertebraten und Algen für eine Baseline des GMR durchgeführt werden, ist wenig Wissen über kleinskalige Variationen in Diversität, Struktur der Lebensgemeinschaften und ökologischen Prozessen unter gegensätzlichen ozeanographischen Bedingungen vorhanden. Um die Auswirkungen solch kleinskaliger Unterschiede in ozeanographischen Verläufen zu untersuchen, wurden zwei Studiengebiete mit Felsriffen vor der Insel Floreana ausgewählt (ungefähr 17 km voneinander entfernt), mit und ohne den Einfluss von Upwelling. Die Struktur der benthischen Lebensgemeinschaften der Untersuchungsstandorte wurde zwei Jahre lang anhand von sublitoralen Monitoring von sessilen Organismen (Algen und Epifauna), mobilen Macroinvertebraten und Rifffischen untersucht. Gleichzeitig wurden an beiden Standorten Sukzessionsstudien und Grazer-Ausschlussexperimente durchgeführt. Weiterhin wurde das Nahrungsnetz von Floreanas Felsriffgemeinschaften mit der Stabilen-Isotopen-Methode analysiert. Es ergaben sich signifikante Unterschiede bezüglich Diversität und Struktur der Lebensgemeinschaften zwischen den Studienorten. Dabei variierte die sessile Lebensgemeinschaft zwischen den beiden Jahreszeiten in dem Gebiet ohne Einfluss von Upwelling. Des Weiteren unterschieden sich die Sukzessionsmuster und Grazing-Effekte zwischen den Standorten. Am Upwelling-Standort wurde eine vorhersagbarere Sukzession offensichtlich, wogegen im Nicht-Upwelling-Gebiet das Sukzessionsmuster eher zufällig war. Die Auswirkung der Grazer auf die Struktur der Lebensgemeinschaft war schwächer am Upwelling-Standort, obwohl dort eine signifikant höhere Anzahl von herbivoren Fischen und Makroinvertebraten festgestellt wurde. Am Standort ohne Upwelling waren trotz einer geringeren Anzahl an Grazern starke Fresseffekte zu beobachten. Daher wurde geschlussfolgert, dass, abhängig von den ozeanographischen Merkmalen, das Ökosystem eher ‘bottom-up’ (Upwelling-Standort) oder mehr ‘top-down’ (Nicht-

IX Zusammenfassung

Upwelling-Standort) gesteuert ist. Weiterhin zeigen die stabilen Isotope, dass das Nahrungsnetz der Felsriffe vor der Insel Floreana aus drei trophischen Ebenen besteht. Diese Ergebnisse wurden mit den Ergebnissen eines trophisch-balancierten Modells verglichen. Schließlich reflektieren die Resultate den besonderen ozeanographischen Rahmen des Galápagos Archipels. Die Insel Floreana repräsentiert somit auch ein „Modell-System“, um ökologische Reaktionen entlang abiotischer Gradienten zu untersuchen. Das Vorkommen von seltenen und bedrohten Arten zusammen mit eingeführten invasiven Arten in den untersuchten sublitoralen Standorten zeigt auch, dass weitere Untersuchungen notwendig sind, um adäquate Managementstrategien mit dem Ziel des Schutzes der einzigarten GMR-Ökosysteme zu entwickeln.

X Resumen

Resumen

Las comunidades de arrecifes rocosos tropicales, son menos prominente que las comunidades de arrecifes de coral, y están caracterizadas por macroalgas, invertebrados móviles, peces de arrecife y diversas comunidades de invertebrados epibentónicos. En la Reserva Marina de Galápagos (RMG), más del 80 % de los hábitats bentónicos poco profundos están dominados por arrecifes rocosos de lava, mientras que los arrecifes de coral son hábitats muy raros. Aún investigaciones acerca de la distribución y abundancia de peces demersales, invertebrados bentónicos y algas han sido realizadas para establecer una línea base de información biológica en la RMG, solo información dispersa sobre la variabilidad de la diversidad, la estructura de la comunidad y procesos ecológicos, bajo condiciones oceanográficas contrastantes a pequeña escala, está disponible. Con el fin de examinar los efectos de las diferencias a pequeña escala bajo diferentes patrones oceanográficos, dos sitios de estudio en arrecifes rocosos de la isla Floreana fueron seleccionados (con una distancia de 17 km, entre sitios), uno con afloramiento y uno no-afloramiento. Cambios en la estructura de la comunidad bentónica en ambos sitios fueron registrados durante dos años, usando técnicas de monitoreo ecológico submareal para organismos sésiles (algas y epifauna), macroinvertebrados móviles y peces de arrecife. Adicionalmente, se realizaron estudios de sucesión béntica y experimentos de exclusión de herbivoría en ambos sitios de estudio. Además un primer estudio de la estructura trófica de la isla Floreana mediante el uso de isótopos estables fue realizado. Los resultados revelaron diferencias significativas entre los sitios de estudio con respecto a la diversidad y estructura de la comunidad. La comunidad de organismos sésiles presentó una variabilidad estacional en el sitio de no-afloramiento. Por otra parte, los patrones de sucesión y los efectos de pastoreo mostraron diferencias entre los dos sitios. En el sitio de afloramiento una sucesión más predecible fue evidente, mientras que los patrones de sucesión fueron más al azar en el sitio de no-afloramiento. El impacto del pastoreo en la estructura de la comunidad fue muy débil bajo condiciones de afloramiento a pesar de presentar una abundancia significativamente mayor de peces y macroinvertebrados herbívoros que en el sitio de no-afloramiento, donde los fuertes efectos de pastoreo fueron evidentes. Por lo tanto, se podría concluir que, dependiendo de las características oceanográficas, el ecosistema esta controlado por procesos de abajo-arriba (sitio de afloramiento) o de

XI Resumen arriba-abajo (sitio de no-afloramiento). Por otra parte, el estudio de isótopos estables reveló que la red trófica del arrecife rocoso de la isla Floreana está compuesta de tres niveles tróficos. Los resultados fueron comparados con los resultados de un modelo trófico. En conclusión, los resultados reflejan el entorno oceanográfico particular del Archipiélago de Galápagos, y confirman que la isla Floreana puede ser considerado como un “sistema modelo” para investigar las respuestas ecológicas a lo largo de gradientes abióticos. La ocurrencia de taxones raros y amenazados junto con las especies exóticas-introducidas en los sitios de arrecifes rocosos estudiados también confirma la necesidad de ampliar las investigaciones con el fin de aplicar estrategias de manejo con el fin de conservar la singularidad de la RMG.

XII Introduction

Introduction

Tropical subtidal rocky reef communities Tropical subtidal rocky reef communities are less prominent than coral reefs and characterized by macroalgae, reef fish, mobile invertebrates and diverse multi-taxa assemblages of epifaunal invertebrates, which encrust rocky reef substrate throughout tropical and sub-tropical regions (Baynes 1999, Jackson 1977, Witman 1992, Witman and Dayton 2001, Witman and Smith 2003). Various oceanographic factors such as currents, upwelling (Connolly and Roughgarden 1998, Kerswell 2006, Underwood and Keough 2001), wave action (Sousa 1979), turbidity (Loya 1976) and sea water temperature (Sanford 1999, Harvell et al. 2002, Southward et al. 2005) influence community structure and diversity. Compared to intertidal habitats, less is known about subtidal communities, mainly due to lower accessibility of potential study sites (Witman and Dayton 2001). But as most impacts of fisheries and threats to biodiversity occur in subtidal habitats (Steneck and Carlton 2000), studies on these communities are urgently needed (Witman and Dayton 2001).

Only few studies on benthic communities in tropical rocky reefs exist, e.g. off the coast of Brazil (Ferreira et al. 2001, Oigman-Pszczol et al. 2004), Panama (Dominici- Arosema and Wolff 2006), Colombia (Zapata and Morales 1997), Costa Rica (Phillips and Perez-Cruet 1984, Dominici-Arosema et al. 2005), Mexico (Arbuto-Oropeza and Balart 2001) and Galápagos (Witman and Smith 2003, Edgar et al. 2004), with the majority of these studies focusing exclusively on reef fish communities. Moreover, tropical subtidal rocky reef communities may have attracted less attention in the past due to the dominance of reef-building coral communities in lower latitudes (Witman and Dayton 2001).

Succession of benthic communities A better knowledge of succession processes of epibenthic communities is essential to understand the dynamics of tropical rocky reefs. The term succession was first coined by Clements (1916) and described as a linear sequence moving towards a climax or end- point community (Clements 1916). Currently, succession is defined as the species replacement during resettlement after a disturbance or the creation of vacant substrata (Sousa and Connell 1992) and is understood as a continuous process with changing

1 Introduction pathways, regulated by biological and physical factors (Noël et al. 2009). It can be initiated when completely virgin substrata are generated (primary succession), e.g. associated with volcanic eruptions or exposure of experimental settlement plates, or by vacant space within an existing community, caused by a disturbance (secondary succession), e.g. grazing pressure or ice scouring (Noël et al. 2009).

There are three different types of succession models described by Connell and Slayter (1977), which explain the interactions between the different settlers during their colonization on vacant space: 1) facilitation, where early colonizers settle on an open space and modify the substratum which is requisite for subsequent development; 2) inhibition, where early stages hinder the settlement of later stages and 3) tolerance, where succession proceeds because of the life history characteristics of the species and not because of interspecific interactions. The occurrence of local disturbances of different intensities resets the developing community to different successional stages and thus creates a patch-mosaic pattern of diversity (Sousa 2001). Generally, biodiversity increases during early succession as new species arrive and settle, but decline during later succession due to the competition of dominant, superior species (Sousa 1979). Overall, biodiversity provides stability, which is also dependent on the differential responses of species to varying conditions (McCann 2000), of productivity (Naeem et al. 1994) of the ecosystem and enhances the probability that a system will perform on a consistent level over a given unit of time (“reliability”, Naeem and Li 1997).

Grazing effects The effects of grazing (top-down) on marine communities are of great interest as changes can cause dramatic impacts on the entire marine system. Top-down effects can be modified by overfishing and the introduction of invasive species (Jackson et al. 2001, Duffy 2003, Castilla et al. 2005, Estes et al. 2011). For instance, in the Caribbean declines of grazers (herbivorous fish and sea urchins) caused phase shifts from corals- to algal-dominated communities (Hughes 1994).

Burkepile and Hay (2006) suggested that the impact of grazers on the abundance and type of algal taxa groups varies with latitude. At lower latitudes, herbivores affected algal community hugely by reducing algal biomass, whereas at higher latitudes, effects varied depending on the productivity of the system. At sites of higher productivity

2 Introduction grazing had little to no effect on species composition, but, in contrast, at sites of low productivity herbivores had strong top-down effects on the diversity of primary producers. For the tropics, Burkepile and Hay (2006) and others (Diaz-Pulido and McCook 2003, Boyer et al. 2004) also showed that grazers can compensate for higher nutrient levels by facilitating grazing-resistant species of algae and decreasing total algal biomass. This suggests that top-down effects are stronger than bottom-up effects. Other studies also described strong grazing impacts on tropical marine systems (Menge and Lubchenco 1981, Burkepile and Hay 2008).

Hixon and Brostoff (1996) outlined three ways in which grazers can change succession: 1) by decreasing the rate of succession (“deceleration”), 2) by increasing the rate of succession (“acceleration”) and 3) by provoking the assemblage to pursue a different pathway. However, it is also possible that grazing may have no effect on the succession process (Farrell 1991, Sousa and Connell 1992).

The impact of herbivory was widely studied for coral reef communities (e.g. Carpenter 1986, Hughes et al. 1987, Hixon and Brostoff 1996, Mumby 2006, Hughes et al. 2007), but information on grazer impacts on tropical shallow rocky reef communities is rare (Irving and Witman 2009, Witman et al. 2010, Brandt et al. 2012).

Food web structure Studying the structure of food webs is important to understand the complexity of interactions in an ecosystem. In order to predict changes in the trophic structure due to changing predator/prey interactions, trophic relationships of key species should be investigated. The stable isotope method demonstrated to be a useful tool to examine food web links (Peterson and Fry 1987, Dauby 1990, Riera et al. 1999, Yoshii 1999, Lepoint et al. 2000). The most suitable elements to compare species positions within a trophic food web of an ecosystem are carbon and nitrogen, as every living organism contains these elements (Post 2002). This approach is based on the fact that the heavy isotopic fraction is increasingly accumulated with each trophic level (Gannes et al. 1998). The carbon isotopic composition contains the information about the carbon source within a trophic chain, whereas the nitrogen isotopic composition is a sufficient tracer for trophic levels (Caut et al. 2009).

3 Introduction

The distribution of species over trophic levels within a benthic community provides important information about hierarchies as well as the transfer of carbon and nitrogen. The length of a trophic chain is influenced by several factors, such as size of the ecosystem and species richness (e.g. Michener and Schell 1994, Lepoint et al. 2000, Abrantes and Sheaves 2009).

The Galápagos Archipelago The Galápagos Archipelago is located in the tropical eastern Pacific Ocean approximately 1000 km west of Ecuador’s mainland. It is comprised of more than 130 large and small islands and islets (Snell et al. 1996) of which four islands, Santa Cruz, San Cristóbal, Isabela and Floreana, are inhabited (Figure 1). The Galápagos Islands are of volcanic origin and emerged from the relatively shallow Galápagos Platform between 60 thousand and 5.6 million years ago (Christie et al. 1992, Geist 1996). To the present, there is still some volcanic activity and eruptions occur repeatedly, such as the volcano Sierra Negra of Isabela Island in 2005 or the eruption of Fernandina in 2009.

-92.0 -91.0 -90.0 SOUTH AMERICA Darwin GALAPAGOS Wolf 1.0 Pinta Marchena

Isabela Genovesa 0.0 Santiago FLOREANA Sta. Cruz Fernandina N -1.0 San Cristóbal

Floreana Española

0 2.5 5 10 km

Figure 1. Map of the Galápagos Archipelago, with focus on Floreana Island.

The Archipelago is situated in a complex oceanographic regime between tropical, subtropical, and upwelling waters (Schaeffer et al. 2008). Here, surface waters from the cold Humboldt Current arrive from the south affecting the southern islands, whereas from the north waters of the warm North Equatorial Countercurrent (NECC) influence

4 Introduction the northern islands (Kessler 2006). These two currents conduce to the effect of the westward flowing South Equatorial Current (SEC) depending on the position of the Intertropical Convergence Zone (ITCZ) (Houvenaghel 1984). This causes the counter flowing strong Equatorial Undercurrent (EUC), which runs from west to east and clashes with the western side of the Archipelago provoking major topographic upwelling of nutrient-rich waters (Chavez and Brusca 1991, Houvenaghel 1984) (Figure 2). Branches of the EUC are responsible for upwelling at smaller scales, e.g. the southwest of Floreana, San Cristobal and the northeast of Santa Cruz. (Schaeffer et al. 2008). Further, topographically induced upwelling occurs at even smaller scale in the form of island wakes (Feldman 1986, Houvenaghel 1978) and internal waves (Witman and Smith 2003). Coupled with the isolated setting of the Galápagos Archipelago, these particular oceanographic circumstances have shaped unique, diverse and complex but poorly understood marine and coastal ecosystems (Houvenaghel 1984, James 1991). The isolation of the Galápagos Archipelago has not only led to diverse ecosystems, but also to a high endemism (19 %) in marine species (Bustamante et al. 2000). However, endemism in marine communities is considerably lower than in terrestrial communities in Galápagos (Tye et al. 2002).

Figure 2. Schematic depiction of the major currents around the Galápagos Islands. The dashed line indicates the limits of the Galápagos Marine Reserve.

5 Introduction

For the Galápagos Archipelago, two major seasons can be distinguished: the cold- dry season from June to November and the hot-wet season from December to April. The environmental variables water and air temperature are closely correlated as well as coastal rainfall and solar exposure (Bustamante et al. 2008). Marine productivity also varies with seasons. Cold, productive waters characterize the cold season, whereas during the hot season productivity is higher (Bustamante et al. 2008). In addition, the Archipelago lies in the centre of El Niño Southern Oscillation (ENSO), a natural large- scale phenomenon that involves oceanographic-atmospheric disruptions varying every 3 to 7 years (Barber and Chavez 1983, Chavez et al. 1999). During the warm El Niño phase the central and east equatorial Pacific Ocean heats and trade winds weaken, resulting in a reduction of upwelling of cold, nutrient-rich waters (Chavez et al. 1999). Under strong El Niño events, such as those of 1982/83 and 1997/98, this may lead to a strikingly decreased primary production (Barber and Chavez 1983). The diminution of food sources affects higher trophic levels, causing a rise in reproductive failure and mortality rates in seabirds like the Galápagos penguin and the flightless cormorant (Valle and Coulter 1987). Pinnipeds such as the Galápagos fur seal and the Galápagos sea lion are affected in the same way (Trillmich and Limberger 1985), and starvation in marine iguana populations has been reported (Laurie 1989). Furthermore, the increase of sea temperature causes bleaching and heightened mortality of corals (Glynn 1988). During the cool La Niña phase strong trade winds lead to an inflow of cold, productive waters boosting the recovery of marine species with the exception of corals, which may be stressed by the extremely cold water temperatures (Rhoades et al. 2009).

Between three and five major biogeographic regions were proposed for the Galápagos Archipelago (Harris 1969, Jennings et al. 1994, Wellington et al. 2001, Edgar et al. 2004). Harris (1969) identified five units based on the distribution and nesting habits of seabirds and on sea temperature. 35 years later, Edgar et al. (2004) reconsidered Harris’ model and suggested three large biogeographic regions: the temperate cold zone (west), the tropical warm zone (far north) and the mixed temperate- subtropical zone (south central/east), based on data of mobile macroinvertebrate and reef fish distribution.

6 Introduction

The Galápagos Marine Reserve (GMR) The Galápagos Islands and their unique and rather pristine ecosystems are of exceptional global value. Hence, the Archipelago was first designated as a World Heritage Site by the UNESCO in 1978. Temporarily, it was added to UNESCO’s “List of World Heritage in Danger” in 2007 due to increasing tourism and immigration to the islands as well as the introduction of invasive species threatening natural habitats. But efforts made by the Ecuadorian government and the Galápagos National Park to limit touristic activities and to restrict immigration were successful and the Galápagos Archipelago was removed from the list in 2010.

In 1998, the Galápagos Marine Reserve (GMR) was established by the Ecuadorian government and, encompassing 133.000 km2, is currently the sixth largest Marine Protected Area in the world (Figure 2). The overall objective of the creation of the GMR was to define and structure uses of the coastal areas in order to reduce conflicts among stakeholders, to extenuate human impacts on sensitive ecosystems and to enhance the sustainability of fisheries (Castrejón and Charles 2013). With the conception of the GMR, industrial fishing was banned and local artisanal fishermen were endowed with exclusive exploitation rights (Castrejón and Charles 2013). Moreover, a multiuse zoning scheme (four subzones: conservation, tourism, fishing and area of special temporary management) was established. Nevertheless, the GMR is subjected to several threats like illegal fishing and shark finning (Viteri and Chávez 2007, Banks et al. 2012), invasive species (Keith, personal communication), pollution by untreated sewage from increasing tourism and growing island populations as well as continuous small oil spills (Banks et al. 2012). In 2001, the Jessica oil spill had severe effects on marine species, especially on the endemic marine iguana (Wikelski et al. 2002). Climatic events such as human induced climate change and the ENSO in combination with the aforementioned local threats may even hinder the recovery of affected communities. For instance, overfishing of predatory reef fishes during and following El Niño events seems to have negative impacts on the recovery of corals, macroalgae and on biodiversity in general (Edgar et al. 2009). Moreover, possible and probable extinctions of some Galápagos marine species are reported (Edgar et al. 2009).

Most of the Galápagos coastline consists of consolidated lava fields with more than 80 % of the shallow benthic habitats being rocky reefs, whereas coral reefs are the rarest

7 Introduction of all shallow habitats in the Archipelago (Bustamante et al. 2008, Banks et al. 2012). Surveys of the distribution and abundance of benthic invertebrates, algae and demersal fish are being conducted to establish baseline information for the GMR (Banks 2003, Banks et al. 2012). But little information is available on species interaction, spatio- temporal variations in diversity and the influence of oceanographic patterns in shaping the benthic community structure, for example of invertebrate species other than corals (Glynn and Wellington 1983, Glynn 1990, 1994, Witman and Smith 2003). An evaluation of the effectiveness of the GMR zoning scheme is in progress and local stakeholders are planning to re-zone the Marine Reserve on the basis of ecosystems function aspects rather than solely on species distribution and diversity aspects.

Shallow reef communities of Floreana Island Floreana Island is the sixth largest island of the Archipelago and lies in the central south region of the GMR (Figure 1), which is the largest biogeographic region. The shallow rocky reefs are characterized by a remarkable, diverse mixing of species originating from Chile-Peru, Mainland Ecuador and central Pacific (James 1991, Edgar et al. 2004). In the past, Floreana consisted of large, well-studied patches of coral reef habitats (Glynn et al. 1979, Wellington 1984), which were depleted by the 1982/83 El Niño event (Glynn 1988). In a few locations around Floreana Island, coral patches and colonies remain, but most of these habitats are decreasing because of high grazing pressure by sea urchins and fish as well as consecutive ENSO stresses (Glynn et al. 1979, Glynn 1990, 1994). A subtidal monitoring program between 2001 and 2003 of 14 sites of Floreana Island revealed spatio-temporal variations in benthic communities between upwelling and non-upwelling areas (Banks 2003). Furthermore, a clear temperature gradient from West to East was evident. It therefore seems that Floreana excels as having greater intra-island variation than other islands and regions of the GMR. Hence, Floreana Island can be regarded as a small-scale example of the larger oceanographic and biogeographic patterns that causes the described differences across the entire archipelago (Banks 2003, Edgar et al. 2004).

8 Introduction

Aim of the thesis The main goal of the present thesis was to investigate the structure and dynamics of benthic communities exposed to upwelling and non-upwelling conditions and their natural succession patterns in shallow rocky reefs of Floreana Island, Galápagos. It further aims to contribute to the understanding of small-scale variability of ecological processes, such as succession trajectories and grazing pressure, in this unique and complex ecosystem.

In addition, it was attempted for the first time to describe the food web structure of Floreana Island by applying the stable isotope approach. To achieve a more complete understanding of the system, a combination of this method with trophic modeling is suggested.

The objectives were:

1) to examine the effects of small-scale differences in oceanographic conditions on diversity and benthic community structure;

2) to investigate the effects of small-scale differences in oceanographic conditions on succession trajectories over a two years period;

3) to identify the grazer community and to examine the effect of grazing pressure under contrasting oceanographic conditions on community composition and diversity;

4) to analyze the food web structure using the stable isotope approach;

5) to interpret the results in the broader context of the marine ecosystems of Galápagos Archipelago and their conservation.

Publication outline This thesis consists of four chapters. The first chapter describes small-scale differences in structure and diversity of rocky reef communities of two sites, an upwelling and a non-upwelling site, off Floreana Island. The second chapter compares the succession pathways of both sites and possible recovery rates of the communities.

9 Introduction

Subsequently, Chapter 3 investigates the grazing impact on the developing communities examined in Chapter 2 by using exclusion treatments. Finally, the stable isotopic signatures of characteristic species of this rocky reef system are analyzed in Chapter 4 in order to obtain information of the trophic structure of the studied communities.

1) Pronounced small-scale differences between Galápagos subtidal rocky reef communities exposed to upwelling and non-upwelling conditions

Authors: Annika Krutwa, Diego J. Ruiz, Matthias Wolff

The idea was developed by A Krutwa with support by M Wolff. Field work and data sampling were carried out by A Krutwa and DJ Ruiz. Data analysis and writing were conducted by A Krutwa with improvements by M Wolff. (under review in Journal of Sea Research)

2) Natural succession patterns on a tropical rocky reef (Galápagos, Ecuador) under upwelling and non-upwelling conditions

Authors: Annika Krutwa, Diego J. Ruiz, Matthias Wolff, Jon D. Witman

The idea was developed by A Krutwa with support by DJ Ruiz and M Wolff. Field work and data sampling were carried out by A Krutwa and DJ Ruiz. Data analysis and writing were conducted by A Krutwa with improvements by M Wolff and JD Witman. (to be submitted to Journal of Experimental Biology and Ecology)

3) Grazing effects on tropical rocky reef communities under upwelling and non- upwelling conditions in Galápagos (Ecuador)

Authors: Annika Krutwa, Diego J. Ruiz, Matthias Wolff

The idea was developed by A Krutwa with support by DJ Ruiz and M Wolff. Field work and data sampling were carried out by A Krutwa and DJ Ruiz. Data analysis and writing were conducted by A Krutwa with improvements by M Wolff. (in preparation for Marine Ecology Progress Series)

4) First insights into the food web structure of a tropical subtidal rocky reef community (Galápagos, Ecuador) using the stable isotope approach

Authors: Carolin M. Herbon, Annika Krutwa

The idea was developed by CM Herbon and A Krutwa. Field and lab work, data analysis and writing were equally conducted by both authors. (under review in Marine Biology Research)

10 Chapter 1 Benthic community structure

1 Pronounced small-scale differences between Galápagos subtidal rocky reef communities exposed to upwelling and non-upwelling conditions

Annika Krutwaa, Diego J. Ruiza,b, Matthias Wolffª

ªLeibniz Center for Tropical Marine Ecology (ZMT) GmbH, Fahrenheitstrasse 6, 28359 Bremen, Germany bCharles Darwin Foundation, Santa Cruz, Galápagos, Ecuador ______

Abstract

The objective of the current study was to examine how small scale differences in oceanographic conditions influence the diversity and composition of subtidal benthic communities off Floreana, a rocky shore island in the central-south of the Galápagos Archipelago. Two study sites 17 km apart were chosen for comparison, a cooler, upwelling and a non-upwelling site, characterized by warmer waters and lower productivity. The community structure was investigated over a 13 month period by subtidal community monitoring. The organism groups studied comprised sessile invertebrates, algae, mobile macroinvertebrates and reef fish. A total of 138 taxa were identified, of which only 56.5 % overlapped between the upwelling and non-upwelling sites. The species composition and diversity of all organism groups considered differed significantly between sites, and seasonal differences were found for the sessile organism community at the non-upwelling site. Our results suggest that seasonal changes in benthic community structure occur in non-upwelling areas of Galápagos as response to the basin-wide cycle of warming and cooling of surface waters associated with the north-south migration of the Intertropical Convergence Zone, while in areas of upwelling, seasonality is suppressed by frequent cold water pulses shaping distinctly adapted benthic communities within short (< 20 km) spatial distances.

Keywords: benthic community structure; Galápagos; rocky reef; seasonality; upwelling ______

11 Chapter 1 Benthic community structure

Introduction

Rocky subtidal benthic communities are less prominent than coral reefs and characterized by macroalgae, mobile invertebrates, demersal fish and diverse multi-taxa communities of epifaunal invertebrates, which encrust rocky substrate throughout tropical and sub-tropical regions (Baynes 1999, Jackson 1977, Witman 1992, Witman and Dayton 2001, Witman and Smith 2003). Oceanographic factors, such as currents, upwelling (Connolly and Roughgarden 1998, Kerswell 2006, Underwood and Keough 2001), wave action (Sousa 1979), water temperature (Harvell et al. 2002, Sanford 1999, Southward et al. 2005) and turbidity (Loya 1976) are reported to influence the structure and diversity of these marine communities.

Communities in areas of high primary productivity are reported to be less diverse than those of oligotrophic systems (Margalef 1997, Rex et al. 2000), and another commonly reported trend for many aquatic taxa is a decrease in species richness from the Equator to the poles (Gray 2001, Rex et al. 1993, Roy et al. 1998). Macpherson (2002) found a positive relationship between benthic diversity and sea surface temperature and, for pelagic species, a negative one with nitrate concentration. Furthermore, it seems that upwelling facilitates recruitment of benthic invertebrates (Connolly and Roughgarden 1998, Roughgarden et al. 1988). However, the primary factors that determine patterns of the structure and diversity of marine communities are still subject of discussion (Gaston 2000, Gotelli et al. 2009, Pennisi 2005, Rosenzweig 1995, Willig et al. 2003).

The Galápagos Marine Reserve (GMR), established in 1998 by the Ecuadorian government, is with an area of 133000 km2 the sixth largest Marine Protected Area in the world. It is located in the Eastern Tropical Pacific, about 1000 km west of Ecuador’s mainland coastline and lies in a complex transition zone between tropical, subtropical, and upwelling waters (Schaeffer et al. 2008). Surface waters from the rather cold Humboldt Current (20 - 22° C) arrive from the south affecting the southern islands, while waters of the warm North Equatorial Countercurrent (NECC) from the north (26 - 29° C) influence the northern islands (Kessler 2006). Depending on the position of the Intertropical Convergence Zone (ITCZ), these two currents contribute to the effect of the westward flowing South Equatorial Current (SEC) (Houvenaghel 1984). This flow

12 Chapter 1 Benthic community structure along the equator causes a counter flow, the strong Equatorial Undercurrent (EUC), which runs from west to east and collides with the western side of the Archipelago provoking major topographic upwelling (Chavez and Brusca 1991, Houvenaghel 1984). Branches of the EUC flowing through the GMR are responsible for upwelling at a smaller scale, e.g. the southwest of Floreana, San Cristobal and the northeast of Santa Cruz, but none of these productive habitats is permanent (Schaeffer et al. 2008). Furthermore, at an even smaller scale, topographically induced upwelling occurs in the form of island wakes (Feldman 1986, Houvenaghel 1978) and internal waves (Witman and Smith 2003). These singular conditions of the GMR have thus shaped complex and poorly understood marine and coastal ecosystems (Houvenaghel 1984, James 1991). Although surveys of the distribution and abundance of benthic invertebrates, algae and demersal fish are being conducted to establish baseline information for the GMR, little information is available on spatio-temporal variations in diversity and the influence of oceanographic patterns in shaping the community structure, for instance of invertebrate species other than corals (Glynn 1994, Glynn 1990, Glynn and Wellington 1983, Witman and Smith 2003).

The island of Floreana is located in the central-south of the GMR and the rocky reefs off Floreana are characterized by a particularly diverse combination of warm- and cool-water biota (Witman and Smith 2003). Banks (2003) presented subtidal monitoring data from 2001 to 2003 of rocky reef habitats of the Galápagos archipelago including 14 sites of the island Floreana, which show spatio-temporal variation in communities within and between upwelling and non-upwelling areas. Further investigations of the within island spatial variation in oceanographic conditions showed a clear temperature gradient from West to East with a warmer, apparently well mixed layer to the north-east and vertically stratified colder waters to the west. Over time scales of hours, the author described temperature changes by up to 8°C at the 15 m isobath. It thus seems that Floreana stands out as having greater intra-island variation than other areas of the Archipelago and can be regarded as a small scale example of the larger oceanographic and biogeographic patterning that causes the observed differences in community structure across the archipelago (Banks 2003, Edgar et al. 2004a).

Upwelling is known to influence the structure of subtidal benthic communities directly by affecting recruitment (Roughgarden et al. 1988), growth of algae

13 Chapter 1 Benthic community structure

(Bustamante et al. 1995) and epifaunal invertebrates (Branch and Griffith 1988), and indirectly by changing the intensity of species interactions (Sanford 1999). While it is commonly known that upwelling areas are of high primary productivity, our knowledge of how upwelling influences the diversity of subtidal communities is still limited (Witman and Smith 2003). According to a review of the relationship between species richness and productivity by Mittelbach et al. (2001) the productivity-diversity relationship can be positive, negative or unimodal, with the latter apparently more common in aquatic studies.

The main objective of the here presented study was to examine whether small-scale differences in oceanographic conditions influence intra-annually the diversity and structure of subtidal benthic communities off the island of Floreana. Two study sites were chosen for comparison, of which the first (“La Botella”) is located at the western part of Floreana and embodies the cooler, upwelling site, whereas at the northeastern part of the island the station “Tres Cuevitas” represents the non-upwelling site, which is characterized by warmer waters and lower productivity. We approached our study by conducting over the period of 13 months, between 2009 and 2010, bimonthly visual underwater censuses of sessile invertebrates, algae, mobile macroinvertebrates and of reef fishes to investigate diversity and species composition as related to the spatially different and temporally changing environmental conditions.

We hypothesize that species abundance and biomass are higher at the upwelling site due to its greater productivity and expect this site to be characterized by a low diversity assemblage of species well-adapted to cold upwelling conditions such as filter feeding ascidians and barnacles. For the non-upwelling site, in contrast, we expect to find a more diverse “tropical” community characterized by species such as zooxanthellate corals. In addition, we expect seasonal differences in community structure at each site. Our results will contribute insights into how the environmental envelope shapes the structure of subtidal benthic communities of Galápagos.

Materials and Methods

Data sampling The study was conducted at two different sites off the island Floreana (Figure 1) between March 2009 and March 2010. The first site, named ‘La Botella’ (LB), is

14 Chapter 1 Benthic community structure situated at the western shore (90º 29' 55.92'' W, 1º 17' 25.16'' S) and is exposed to strong upwelling (Witman et al., 2010). The second site, ‘Tres Cuevitas’ (TC) is located on the northeast side of the island (90º 24' 30.26'' W, 1º 14' 6.45'' S) and represents a non- upwelling site with warmer waters and a well-mixed layer (Banks 2003). The two sites are nearly 17 km distant from each other. LB is characterized by a vertical rocky wall that falls at approx. 12-15 m depth in a horizontal rocky reef with irregularly occurring patches of sand. The site TC consists of a slightly sloping rocky reef with increasing sandy sediment patches with depth. Both sites are characterized by rough lava rocky reefs which show high structural complexity.

90º30’ S 90º25’ S90º20’ S

FLOREANA ISLAND GALAPAGOS S ’ 100 m N 1º 10 50 m 1

S 20 m ’ 1º15

2

50 m m 50 50

20 m 20 20 m 20 Island S ’ Study sites

1º20 Iso-bathimetry

100 m m 100 100 S ’ 1º25

1 Tres Cuevitas 2 La Botella

20 m 20 m

20 m

Figure 1. Study sites: Tres Cuevitas (TC) and La Botella (LB).

15 Chapter 1 Benthic community structure

At each site a submarine temperature logger (HOBO Pro v2) was attached at 15 m to record the temperature at 10-min intervals throughout the study and afterwards until March 2011.

Visual underwater censuses of benthic marine communities were carried out bimonthly at each site by three divers along randomly established 50 m transects at 15 m. Between March 2009 and March 2010, seven field trips were conducted. The studied organism groups comprised sessile invertebrates and algae, mobile macroinvertebrates and reef fish. Percentage cover of sessile invertebrates and algae was estimated through a 0.5 x 0.5 m quadrant with 81 intersection points spaced randomly at 5 m intervals along the 50 m transect line. The benthic species or substrate lying under each intersection point was recorded as one point and thus percent coverage was calculated by quadrant. Mobile macroinvertebrate species occurrence and abundance values were obtained within a 1 m corridor at both sides every 25 m along the 50 m transect yielding 4 replicates per census. Reef fish species, abundances and size ranges were registered along a 5 m2 corridor on both sides of the 50 m transect, resulting in a total of 500 m2 area coverage per transect.

Data analysis All statistical analyses were conducted separately for each studied group/community. Univariate statistical analyses were carried out with the programs Statistica 6 and PAST 2.17. Data were tested for normal distribution (Shapiro-Wilk test) and for homogeneity of variances (Levene’s test). Data that were homogeneous and normally distributed were analyzed with the t-test (P < 0.05). Diversity of fish, mobile macroinvertebrate and sessile community at all locations was expressed with the Shannon Diversity Index (H’) and the Pielou Eveness (J’) and tested for significant differences between sites by bootstrapping (Buckland et al. 2005, Hammer 2012).

Fish biomass was estimated from abundance counts and size estimates using length- weight relationships (Fulton 2007, Ricker 1975) provided for the total length of each fish species (in some cases genus) in Fishbase (www.fishbase.org). Bias in diver’s perception of fish size underwater was additionally corrected using relationships presented in Edgar et al. (2004b).

16 Chapter 1 Benthic community structure

The statistical program Primer 6 (Primer-E Ltd.) was used to analyze ecological differences between locations and seasons for each studied group. Differences in community structure were initially described using multidimensional scaling (MDS). In order to analyze changes in percent cover of sessile community and density of mobile macroinvertebrates each community was separated into taxonomic/functional groups and analyzed as follows: the sessile community was divided into calcareous algae, encrusting algae, filamentous algae and macroalgae, and the macroinvertebrate community into asteroids and echinoids. All data were fourth-root transformed to lower the influence of dominant species and to increase the weight of rare species. Further, analyses were based on Bray-Curtis similarity indices. The significance of differences between the fixed factors location and season was tested using the permutational multivariate analysis of variance PERMANOVA (Anderson et al. 2008). Post-hoc PERMANOVA pair-wise tests were carried out to detect differences within levels of each relevant interaction.

Due to the lack of replicates for each fish monitoring data, samples were grouped by season, then site and seasonal differences of total biomass of reef fish were tested.

Results

Temperature Temperature showed seasonal variability at both locations (Figure 2). The temperature profile in figure 2 demonstrates well-defined warm and cold periods from 2009 until the beginning of 2011. Mean temperature at TC was with 22.47º C, 0.91° C higher than at LB (Table 1). Maximum and minimum recorded temperatures during the study were 28.22° C and 14.02° C at LB in 2010. Unfortunately, the temperature logger at TC did not record the water temperature between the beginning of December 2009 and the beginning of April 2010, therefore missing data were approximated by a linear regression model using temperature logger data from 6 m and 15 m depth at TC (R2 = 0.9728; n = 22; Figure A1). Mean temperature variations were higher at the upwelling site LB (Table 1).

17 Chapter 1 Benthic community structure

La Botella (LB) Tres Cuevitas (TC) 28 26 24 22 20 18

Temperature (ºC) 16 14 3945678 10111212345678 9 1011 1212

2009 2010 2011 Year Figure 2. Temperature profile at TC and LB from March 2009 to March 2011; thick line: monthly average, thin line: daily average.

Table 1. Water temperature statistics (in °C).

La Botella (LB) Tres Cuevitas (TC) Average temperature (± SD) 21.56 ± 2.75 22.47 ± 2.24 Maximum daily temperature 28.22 28.15 Minimum daily temperature 14.03 14.67 Temperature range 14.19 13.48 Mean temperature variation Daily 2.20 1.80 Weekly 2.50 2.20

Species number and diversity During the study a total of 138 species and taxonomic groups, respectively, were observed at both sites, of which 44 were sessile invertebrates, 25 algae, 21 mobile macroinvertebrates and 55 fish species. At LB 28 species of sessile invertebrates and 18 of algae occurred together with 16 species of mobile macroinvertebrates and 43 fish species. At TC we recorded 31 species of sessile invertebrates, 20 of algae, 15 of mobile macroinvertebrates and 39 fish species. At all sites we observed cyanobacteria whereas dead coral was only found at TC (see Table A1 species list). Both areas had 78 species in common (56.5 %).

Significant differences in Shannon diversity and Pilou Eveness were found between the two sites (Table 2). Shannon diversity, Pilou Eveness and species numbers (except for fish species) were higher at TC than at LB. However, differences in species number were not significant.

18

Chapter 1 Benthic Benthic 1 Chapter

Table 2. Means of univariate measures of fish, mobile macroinvertebrate and fish community structure at LB and TC. S: Species/taxa number (± SD); H’: Shannon diversity and J’: Pilou Evenness (95 % bootstrap confidence interval). P-values for S by t-test; for H’ and J’ by bootstrap test.

Sessile community Macroinvertebrates Fish LB TC P LB TC P LB TC P 21.3 23.6 0.13 4.3 5 0.36 19.7 16.3 0.16 S (2.8) (2.4) (t12 = -1.64) (1.4) (1.4) (t12=-0.96) (4.8) (2.7) (t12 = 1.52) 1.71 2.44 0.16 0.69 2.09 2.62 H’ 0.001 0.001 0.001 (1.53; 2.01) (1.54; 2.0) (0.13; 0.31) (0.05; 0.37) (2.36; 2.57) (2.28; 2.49) 0.12 0.24 0.11 0.2 0.18 0.35 J’ 0.042 0.927 0.007 (0.38; 0.59) (0.38; 0.59) (0.1; 0.17) (0.2; 0.55) (0.23; 0.28) (0.31; 0.4) 19

community structurecommunity Chapter 1 Benthic community structure

Community analyses MDS plots show spatial differences in fish, mobile macroinvertebrates and sessile species community structure between sites and surveys (Figure 3). PERMANOVA indicates significant differences between locations for macroinvertebrates and the sessile community (P < 0.001), which also varied significantly between seasons (P < 0.05; Table 3). Post-hoc pair-wise tests revealed significant differences between seasons at TC (P = 0.048) for the sessile community.

2D Stress: 0,01 2D Stress: 0,16 2D Stress: 0,13 LB TC

ABC Figure 3. MDS ordination depicting relationship of monitored sites and surveys; A) sessile community, B) macroinvertebrate community, C) fish community.

Table 3. Results of PERMANOVA main test for macroinvertebrate and sessile community.

Dataset Source Location Season Location × season Macroinvertebrate d.f. 1 1 1 community MS 11383 859.72 198 Pseudo-F 21.862 1.6511 0.38027

P(perm) 0.001 0.204 0.749 Sessile d.f. 1 1 1 community MS 69161 3614.2 2155.5 Pseudo-F 40.446 2.1136 1.2606

P(perm) 0.001 0.03 0.265 Percent cover, density and biomass At LB calcareous algae (66 %), encrusting algae (12 %) and macroalgae (6 %) dominated the sessile community, whereas at TC hard corals (34 %), calcareous algae (26 %) and filamentous algae (18 %) were the most abundant groups. At LB hard corals were lacking completely. Seasonal changes in percent cover of the sessile community are shown in figure 4 for the four most abundant taxonomic groups mentioned above excluding hard corals. PERMANOVA main test showed significant differences between both sites for all four groups. However, a significant seasonal change in percent cover was evident only for encrusting and filamentous algae (P < 0.05; Table A2).

20 Chapter 1 Benthic community structure

Changes in densities per 50 m2 of the two main macroinvertebrate groups are shown in figure 4. Echinoid density was significantly higher at LB than at TC, whereas asteroid density showed nearly significant differences (P = 0.051) between sites with higher densities at TC. Even so, no significant differences between seasons were found (Table A3).

Fish biomasses are significantly higher at LB than at TC (P = 0.002, Table A4), but seasonality was not obvious (Figure 4).

Calcareous algae Fish 75 90 60 hot cold 80 45 70

30 2 15 60 0 50

kg/250m 40 Filamentous algae 30 30 25 20 20 10 15 10 0 5 0 Echinoids Encrusting algae 400

20 2

Coverage (%) 300 15 200 10 100 5 Number/50m 0 0

Macroalgae Asteroids 15 5 2 4 10 3 5 2 1 Number/m 0 0 LB15 TC15 LB15 TC15 Figure 4. Changes in percent cover, density and biomass (mean ± SE) of the main functional groups between seasons.

Discussion

The island of Floreana clearly shows differences in community composition between sites. These site-distinct patterns reflect observed oceanographic differences and shall be discussed in the following.

The temperature profiles of both sites show two distinct seasons during our study and beyond. In Galápagos the seasonal variability is dominated by a basin-wide cycle of warming and cooling of surface waters associated with the north-south migration of the intertropical convergence zone (Palacios 2004). Since Galápagos is located near the

21 Chapter 1 Benthic community structure centre of the most intense ENSO events (Glynn and Ault 2000, Wolff 2010), this seasonal cycle is further modulated by the prevailing ENSO regime in the region. The comparison of the temperature trajectories recorded at both sites and during the period of 2009 to 2011 clearly revealed that the upwelling site LB was characterized by lower mean (21.56° C) and minimum temperatures (14.03° C) due to upwelling processes (Witman et al. 2010). However, from December 2009 to January 2010 temperatures at the cool, upwelling site even surpassed those of the warm site TC with a maximum difference of 0.81º C, most probably due to the lack of upwelling at LB and the absence of moderate currents during these months. Nevertheless, daily and weekly mean temperature variations were still 22 % and 14 % higher at LB than at TC indicating stronger gradients over short time intervals (Fig. 2). Interestingly, the following year of the study (beginning of 2010) showed even more pronounced seasons with stronger temperature extremes. There, monthly mean temperatures remained below 18° C at LB and 20° C at TC for more than four months in contrast to 2009, when monthly mean temperatures stayed above 18° C (LB) and 20° C (TC), respectively and the cold period was limited to about two months only.

As hypothesized, Shannon diversity and Pilou Evenness were higher for all organism groups studied at the warmer, non-upwelling site TC. However, species richness did not differ significantly between sites. So what differs are the relative proportions of specimens of the different species, with few numerically dominating (e.g. Eucidaris galapagensis), and many rare species at LB and a much higher number of abundant species at TC. Further, at both sites we could observe common species, which are widely distributed in the GMR and well adapted to changing oceanographic conditions such as, the Galápagos ringtail damselfish, the slate-pencil sea urchin as well as the algae Ulva spp. and Lithothamnium spp. (Glynn et al. 1979, Ruttenberg et al. 2005). However, more than 40 % of the species were just found at one site or the other, despite their relative proximity. For example, zooxanthellate corals like Pavona gigantea and P. clavus occurred only at the non-upwelling, warmer site TC. In contrast, colonies of P. gigantea were also found at upwelling sites in the Gulf of Panamá, where they show seasonality in reproduction (Glynn et al. 1996). At LB, strong and frequent upwelling events throughout the year and extreme temperature gradients (as recorded for 2010 and 2011) seem to hinder the settlement of species such as P. gigantea, which reproduce in non-upwelling periods (after the upwelling season), when water

22 Chapter 1 Benthic community structure temperatures are high (Glynn et al. 1996). Further, the rather subtropical sponge Cliona chilensis, which is widely distributed along the Patagonian shelf (Van Soest 2013), was only found at the upwelling site LB. The exclusive occurrence of those two species at only one of the study sites reflects the observed oceanographic differences between both sites.

Edgar et al. (2004a) described for Galápagos fish and macroinvertebrate communities, that regions with the lowest overall species richness possess a temperate rather than a tropical climate and Connel and Irving (2008) demonstrated that patterns of regional diversity are related to regional variability in productivity and consumption. At smaller scales, Kotta and Witman (2009) outlined that environmental disturbance and productivity modulate diversity patterns and that this is limited by the size of the regional species pool. It thus seems that the observed higher diversity at the warm TC site of Floreana agrees with the general statement of Edgar et al. (2004a), with regard to temperate-tropical gradients in community characteristics in Galápagos. However, in our case it is the species diversity and not the species richness that is higher at the warm site. This is mainly due to between-site differences in the relative numeric rank position of the species, which would also suggest differences in community interactions between sites.

Our study clearly shows that spatial differences in the structure of subtidal benthic communities off Floreana exist between the upwelling site LB and the non-upwelling site TC.

The macroinvertebrate community is dominated by E. galapagensis, which is the most abundant sea urchin species in the central part of Galápagos (Brandt and Guarderas 2002) and, at high densities influences the structure of benthic communities (Brandt 2003, Glynn and Wellington 1983). Densities of this species are significantly higher at LB, as well as the biomass of its predator, the hogfish Bodianus diplotaenia (Krutwa et al. unpublished data), which may thus play a key role in shaping the community at this site. In contrast, Sonnenholzner et al. (2009) described a E. galapagensis - predator - algae relationship, where non-coralline algae cover was decreased by grazing through highly abundant E. galapagensis and algae cover increased when predators were present and decreased sea urchin densities. Additionally, E. galapagensis shows nocturnal behavior (Dee et al. 2012). As surveys were conducted

23 Chapter 1 Benthic community structure during daylight, sea urchin density may have thus even been underestimated. Asteroid density, on the contrary, was higher at the non-upwelling site TC. Asteroids are known to adapt easily to changes in food availability due to their diversified feeding (Hickman 1998), which may allow them more easily to persist conditions of lower food productivity at TC. This also holds for echinoids which are among the key grazers off tropical coasts (Lawrence 1975, Witman and Dayton 2001).

If we look at seasonal changes at both sites, macroinvertebrates did not show any significant ones neither with regard to species composition nor density. The dominant pencil sea urchin E. galapagensis is known to be highly adapted to changes in oceanographic conditions (Glynn 1994). As an omnivore and bioeroder, which grazes on encrusting algae but also feeds on corals like Pocillipora and Pavona (Glynn et al. 1979, Hickman 1998), this species may therefore be able to easily adapt to changes in type and quantity of natural food supply. Due to its dominance at both locations, macroinvertebrate community structure does not seem to vary seasonally.

For the sessile organisms, community differences between sites were significant at each point in time mainly because of the presence of hard corals at the warmer site TC, which contributed 34 % to benthic cover here. In contrast, at the upwelling site LB hard corals are completely lacking probably due to frequent strong upwelling events in this area (Witman et al. 2010). Significant differences between the warm and the cold season were found only at the non-upwelling site TC. During the cold season we observed the unpalatable brown algae Padina spp. which occurred widely at TC and therefore possibly affecting sessile community composition. In contrast, sessile community structure remained the same during the cold and the warm season at the upwelling site LB, supposedly due to both the lower seasonal temperature extremes here and the frequent upwelling events throughout the year which shape communities that are well-adapted to more frequent temperature variation. Thus, temperature seems to influence sessile community patterning at a significant scale. Surprisingly, percent cover of filter feeding organisms remained under 2 % at both sites, possibly due to competition for space with algae (Miller and Etter 2008, Witman and Dayton 2001). On vertical rock walls at Galápagos upwelling sites (such as our site LB) filter feeding invertebrates dominate in percent cover (Witman et al. 2010, Witman and Smith 2003,

24 Chapter 1 Benthic community structure personal observation), since they can easily outcompete algae, which may not be able to survive unfavorable light conditions.

Algae cover differed significantly between both sites. The most dominant species in the group of calcareous algae was Lithothamnium spp., which was found at all studied sites with higher densities at the upwelling site LB. Encrusting algae were the second most abundant group occurring there but played a minor part at the warmer site TC suggesting that species within this functional group tend to propagate better under cooler conditions (Kaehler and Williams 1996). This may also explain the significant seasonal differences in percentage cover of encrusting algae. We found even higher densities of grazing echinoids at the upwelling site. Surprisingly, filamentous algae coverage was significantly higher at the non-upwelling site TC. For Galápagos, Kendrik (1991) described an increase in percent cover of filamentous species with an increase in water movement. In this study observations were contrasting. At LB upwelling events occur frequently and hence, water perturbations are of higher magnitude than at TC. Thus, at TC higher percent cover of filamentous algae may be due to a significant lower number of grazers (sea urchins). However, findings by Kendrik (1991) may explain the significant increase in algal cover during the cold season, when wind and currents cause enhanced water movements.

Macroalgae cover was also significantly higher at TC than at the upwelling site LB and can also be explained by less herbivory at this site (Hughes et al. 1987). Although an increase of macroalgae coverage was observed during the cold season it was not statistically significant. However, changes in macroalgae cover is known as a response to seasonal cycles (Diaz-Pulido and Garzón-Ferreira 2002, Prathep et al. 2007), but also herbivory and disturbance (Mumby et al. 2005, Vroom et al. 2005).

Significant differences in fish community structure between both sites may be explained by a considerable proportion of planktivore fish biomass (14 %) at the upwelling site LB compared with a negligible proportion of 1 % at TC (Krutwa et al., unpublished data). At LB cold nutrient-rich waters are upwelled and facilitate plankton production (Gonzalez-Rodriguez 1992), providing a rich food resource for planktivore fish. The significantly higher fish biomass found at LB compared to TC confirms previous assumptions that higher biomass at the upwelling site is due to the higher productivity of the system (Daneri et al. 2000, Schaeffer et al. 2008).

25 Chapter 1 Benthic community structure

It is known that the Galápagos marine environments are extremely variable not only in space but also over time (Edgar et al. 2009, Bustamante et al. 2008, Bustamante et al. 2002, Vinueza et al. 2006) and hence, this highly dynamic system makes trends e.g. in biodiversity difficult to monitor (Bustamante et al. 2002). For example, Witman and Smith (2003) described a rapid community change at an upwelling site in Galápagos within a year. Although differences in community structure between the wider biogeographic regions of Galápagos were reported to show clear patterns (Banks 2003, Edgar et al. 2004a), our study is the first to provide evidence that the subtidal community structure may even substantially differ over very small distances (< 20 km). These findings also imply that community monitoring on the scale of the Galápagos Archipelago needs to account for these fine scale differences, by considering an adequate spacing and number of sample replicates distributed over the archipelago.

Conclusion

The GMR is a highly complex and dynamic system, where spatial and temporal variation of subtidal benthic communities does not only occur between larger biogeographic regions (Danulat and Edgar 2002, Edgar et al. 2004a) but also on a small scale of a few kilometers within a single region. Communities of the island of Floreana differ between the upwelling site LB and the non-upwelling site TC. Shannon diversity was significantly higher at TC for all organism groups. Significant seasonal differences in sessile community composition were only found at the warm site, where seasonal temperature change was more pronounced, whereas at the upwelling site the sessile community appears more adapted to temperature changes. The mobile macroinvertebrate community seems to be the most adapted group in this study and did not show temporal variations at all. Reef fish biomass remained the same during the cold and the warm season but differed significantly between upwelling and non- upwelling.

While the observed spatial and temporal differences appear to be related to both temperature and productivity, further studies on biotic interactions, succession processes and species physiology have to be conducted, and oceanographic patterns should be investigated more in detail (e.g. change of turbidity, currents, chlorophyll and nutrients). All together, the species composition, their relative abundances, their interactions, and

26 Chapter 1 Benthic community structure their spatial and temporal variation concur to the resilience of the benthic ecosystem (Chapin et al. 2000), thus making it necessary to understand subtidal benthic community structure in ecosystem performance and environmental change.

Acknowledgments

We thank the Charles Darwin Foundation and the Galápagos National Park Service. Consequently, we thank S. Banks for his support and impulses. AK acknowledges the DAAD for being awarded a scholarship. Special thanks go to R. Pepolas, J. Delgado, J. Moreno, N. Tirado, J. Suarez, S. Clarke, A. Schuhbauer, D. Sabando, R. Sanzogni who helped during the field work.

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Appendix

27 26 25 24 23 22 21 20 y = 0,9454x + 0,676 temperature TC 15 m (C°) TC temperature 19 2 R = 0,9728 18 18 19 20 21 22 23 24 25 26 27 temperature TC 6 m (C°)

Figure A1. Regression between monthly means of water temperature at 6 m and 15 m at study site TC (n = 22).

34 Chapter 1 Benthic community structure

Table A1. Species list.

Tres Cuevitas La Botella Sessile organisms Antipathes galapagensis x Aplidium solidum x Aplidium spp x x Ascidia spp x x Astrangia browni x Bryopsis spp x x Bugula cf. californica x x Bugula neritina x x Bunodosoma grandis x Cyanobacteria x x Ciocalypta spp x x Cladopsammia eguchii x Cleidochasma porcellanum x Cliona chilensis x Corallina spp x Diatoms x x Didemnum spp x x Eudistoma spp x Filamentous brown algae x x Filamentous green algae x x Filamentous red algae x x Gymnogongrus spp x x Schizymenia ecuadoreana x Hildenbrandia spp x x Hipponix spp x x Hippoporina verrilli x x Hypnea spp x x Isognomon recognitus x Jania spp x x Lichenopora intricata x Lithothamnium spp x x Macrorhynchia philippina x Megabalanus peninsularis x x Megalomma mushaensis x x Membranipora arborescens x x Nitophyllum spp x x Obelia dichotoma x x Orange sponge x x Oulangia bradleyi x Padina spp x x Pavona clavus x Pavona gigantea x

35 Chapter 1 Benthic community structure

Table A1. continuation…

Tres Cuevitas La Botella Sessile organisms Pocockiella spp x x Porites lobata x Psammocora spp x Pterocladia spp x Pterosiphonia spp x x Pyura cf. haustor x x Ralfsia spp x Rhodymenia spp x Rhynchozoon rostratum x x Salmacina tribranchiata x x Serpulorbis margaritaceus x x Spatoglossum spp x Spirobranchus giganteus x x Tubastraea coccinea x Tubiculous polychaete x x Ulva spp x x Unidentified brown algae x Unidentified bryozoan x Unidentified hydroid x x Unidentified red algae x x White sponge x Mobile macroinvertebrates Centrostephanus coronatus x x Columbella haemastoma x x Conus nux x Conus purpurascens x Coronaster marchenus x Eucidaris galapagensis x x Hexaplex princeps x x Holothuria fuscocinerea x Holothuria kefersteini x Isostichopus fuscus x x Latirus sanguineus x Leucozonia tuberculata x Linckia columbiae x Mithrodia bradleyi x Muricopsis zeteki x x Nidorellia armata x x Pentaceraster cumingi x x Pharia pyramidata x Phataria unifascialis x x Pleuroploca princeps x Scyllarides astori x

36 Chapter 1 Benthic community structure

Table A1. continuation…

Tres Cuevitas La Botella Fish Alphestes immaculatus x Anisotremus interruptus x x Apogon atradorsatus x x Aulostomus chinensis x x Bodianus diplotaenia x x Bodianus eclancheri x Calamus taurinus x Canthigaster punctatissima x Cephalopholis panamensis x x Chromis atrilobata x x Cirrhitichthys oxycephalus x x Cirrhitus rivulatus x Dasyatis brevis x x Decapterus muroadsi x x Dermatolepis dermatolepis x Diodon holocanthus x Epinephelus labriformis x x Fistularia commersonii x x Girella freminvillei x x Halichoeres dispilus x x Halichoeres nicholsi x x Heterodontus quoyi x Holacanthus passer x x Hypsoblennius brevipinnis x Johnrandallia nigrirostris x x Labrisomus dendriticus x x Lutjanus argentiventris x Lutjanus viridis x Microspathodon dorsalis x Muraena argus x Mycteroperca olfax x x Myrichthys tigrinus x Nicholsina denticulata x x Ophioblennius steindachneri x x Orthopristis forbesi x x Paralabrax albomaculatus x Paranthias colonus x x Plagiotremus azaleus x x Prionurus laticlavius x x Rypticus nigripinnis x Scarus ghobban x x Scomberomorus sierra x Scorpaena plumieri mystes x

37 Chapter 1 Benthic community structure

Table A1. continuation…

Tres Cuevitas La Botella Fish Sectator ocyurus x Semicossyphus darwini x x Seriola rivuliana x x Serranus psittacinus x x Sphoeroides annulatus x x Sphyraena idiastes x Stegastes leucorus beebei x x Sufflamen verres x x Taeniura meyeni x Thalassoma lucasanum x x Xenocys jessiae x Zanclus cornutus x

38 Chapter 1 Benthic community structure

Table A2. Results of PERMANOVA main test for total cover of calcareous algae, encrusting algae, filamentous algae and macroalgae.

Dataset Source Location Season Location × season Calcareous algae d.f. 1 1 1 MS 615.04 6.1929 7.1771 Pseudo-F 65.387 0.6584 0.76303 P(perm) 0.001 0.405 0.377 Encrusting algae d.f. 1 1 1 MS 260.14 41.119 5.3623 Pseudo-F 36.727 5.8053 0.75707 P(perm) 0.001 0.021 0.373 Filamentous algae d.f. 1 1 1 MS 68.568 143.25 0.23879 Pseudo-F 6.2396 13.036 0.02173 P(perm) 0.015 0.001 0.88 Macroalgae d.f. 1 1 1 MS 734.72 197.77 170.96 Pseudo-F 4.8374 1.3021 1.1256 P(perm) 0.019 0.241 0.306

Table A3. Results of PERMANOVA main test for total density of asteroids and echinoids.

Dataset Source Location Season Location × season Asteroids d.f. 1 1 1 MS 114.13 63.602 1.3085 Pseudo-F 3.8092 2.1228 0.04367 P(perm) 0.051 0.166 0.852 Echinoids d.f. 1 1 1 MS 6743.9 18.142 10.313 Pseudo-F 366.47 0.98588 0.56039 P(perm) 0.001 0.316 0.484

Table A4. Results of PERMANOVA main test for total fish biomass.

Dataset Source Location Season Location × season Fish d.f. 1 1 1 MS 1127.7 0.82484 1.1292 Pseudo-F 18.225 0.01333 0.018249 P(perm) 0.002 0.968 0.959

39

40 Chapter 2 Natural succession

2 Natural succession patterns on a tropical rocky reef (Galápagos, Ecuador) under upwelling and non-upwelling conditions

Annika Krutwaa, Diego J. Ruiza, Matthias Wolffa, Jon D. Witmanb aLeibniz Center for Tropical Marine Ecology (ZMT) GmbH, Fahrenheitstrasse 6, 28359 Bremen, Germany bBrown University, Providence, RI 02912 USA ______

Abstract

The succession of tropical subtidal rocky reef communities was investigated for two years at an upwelling and non-upwelling site off the island of Floreana (Galápagos) using natural lava substrate as settlement plates. Results show a more predictable succession at the upwelling site, whereas succession at the non-upwelling site was more random. Communities at the upwelling site assembled relatively quickly as the community resembled the surrounding natural community after two years. Assembly took longer at the non-upwelling site because of low recruitment rates and slowly growing hard corals, which form an important part of the community. While species richness did not differ significantly between upwelling and non-upwelling sites after two years, the species composition and relative abundance of the contributing taxa varied between sites over the succession trajectories. Dominant species accounting for the differences in community succession between sites were the crustose algae Lithothamnium spp. and Hildenbrandia spp. at the upwelling site as well as the foliose algae Ulva spp. and green filamentous algae at the non-upwelling site. These different patterns of succession demonstrate the high variability of ecological processes allied with oceanography within a single biogeographic region. Since community structure of natural and developing assemblages differed at the conclusion of the experiment it is likely that more than two years will be required for benthic communities to recover from physical and biological disturbances opening up space on subtidal volcanic substrate in the Galapagos Marine Reserve.

Keywords: Galápagos; natural substratum; rocky subtidal; succession; tropical rocky reef; upwelling vs. non-upwelling ______

41 Chapter 2 Natural succession

Introduction

Tropical rocky reefs are less conspicuous and compared to the three main tropical marine systems; coral reefs, mangroves and seagrass beds, little information is available regarding community composition and ecological processes (Hatcher et al. 1989, Baynes 1999, Witman and Smith 2003, Dominici-Arosema and Wolff 2006). Therefore, a better knowledge of succession processes of epibenthic communities is crucial to understand the dynamics of tropical rocky reefs. The term succession, first coined by Clements (1916), was described as a linear sequence moving towards a climax or end- point community (Clements 1916). Presently, succession is defined as the species replacement during resettlement after a disturbance or the creation of vacant substrata (Sousa and Connell 1992). However, nowadays succession is understood as a continuous process with changing trajectories, influenced by biological as well as physical factors (Noël et al. 2009). The occurrence of local disturbances of different intensities resets the developing community to different successional stages and thus creates a patch-mosaic pattern of diversity (Sousa 2001). Generally, biodiversity increases during early succession as new species arrive and settle, but decline during later succession due to the competition of dominant, superior species (Sousa 1979). Biodiversity may enhance stability (McCann 2000), which is also dependent on the differential responses of species to varying conditions of productivity (Naeem et al. 1994) of the ecosystem and enhances the probability that a system will perform on a consistent level over a given unit of time (“reliability”, Naeem and Li 1997).

Most of the knowledge of benthic succession processes derives from intertidal rocky communities (Menge 1975, Dean and Connell 1987a,b,c, Anderson and Underwood 1994, Farrell 1991, Foster et al. 2003), or from recruitment panels installed on shallow structures such as pontoons, rafts, piers etc. (Anderson and Underwood 1994, Brown and Swearingen 1998, Altman and Whitlatch 2007, Canning-Clode et al. 2008, 2009). Succession on artificial substrata (Olabarria 2002) may differ from that on naturally occurring subtidal rocky reefs (Connell and Glasby 1999, Glasby 2011, Glasby and Connell 2001). Less information is available regarding succession patterns of subtidal rocky reef communities (Witman 1987, Vance 1988, Watson and Barnes 2004 a,b; Antoniadou et al. 2010). Moreover, the majority of succession studies on subtidal rocky

42 Chapter 2 Natural succession reef habitat have been carried out in subtropical, temperate or polar ecosystems (Breitburg 1985, Fricke et al. 2008, Antoniadou et al. 2011). Recently, studies in upwelling systems were conducted to examine the influence of high productivity conditions on community development (Cifuentes et al. 2007, Cifuentes et al. 2010, Pacheco et al. 2011). Knowledge of succession in tropical benthic communities is limited (Baynes 1999). In addition, the influence of seasonal or constant upwelling on succession processes in subtidal tropical rocky reef communities has not been studied in any detail.

The Galápagos Archipelago located in the Eastern Tropical Pacific about 1000 km west of the coast of Ecuador lies in a complex transition zone between tropical, subtropical, and upwelling waters (Schaeffer et al. 2008). Here, surface waters from the cold Humboldt Current (20-22°C) arrive from the south affecting the southern islands, while waters of the warm North Equatorial Countercurrent (NECC) (26-29°C) influence the northern islands (Kessler 2006). These two currents change in relative strength and position with the position of the Intertropical Convergence Zone (ITCZ) and contribute to the effect of the westward flowing South Equatorial Current (SEC) (Houvenaghel 1984). The SEC causes a counter flow, named the strong Equatorial Undercurrent (EUC), which flows from west to east and clashes with the western side of the Galápagos archipelago, which provokes major topographic upwelling (Chavez and Brusca 1991, Houvenaghel 1984). Branches of the EUC running through the Archipelago are frequently present and in combination with internal waves responsible for upwelling at smaller scales in the central Archipelago (e.g. the strong upwelling sites La Botella, Cuatro Hermanos, Gordon Rocks etc.) and locations of strong upwelling are predicted by the topography offshore (Witman et al. 2010). This singular oceanographic setting of the Galápagos Islands has formed a complex and poorly understood set of marine and coastal ecosystems (Houvenaghel 1984, James 1991). In the past, studies on spatio-temporal variations in diversity and on the influence of oceanographic patterns in shaping the community structure was mainly focused on corals (Glynn 1994, Glynn 1990; Glynn and Wellington 1983) and less on other invertebrates (Witman and Smith 2003) or algae (Graham et al. 2007). Findings of Witman and Smith (2003) in the Galápagos suggested a particularly rapid turnover of diversity and biomass at tropical upwelling sites with one of the “fastest diversity increases in any subtidal epifaunal community” (Witman 1992, Connell 1997, Smith and Witman 1999). Further,

43 Chapter 2 Natural succession upwelling is associated with high recruitment and abundance of the barnacle Megabalanus spp., which as an important prey species creates a bottom up effect in the food web (Witman et al. 2010). However, more information on benthic succession in the tropics is required, to better understand the magnitude and direction of environmental impacts.

To study succession patterns of subtidal rocky reef communities under upwelling and non-upwelling conditions we chose the shallow rocky reefs off the island of Floreana, located in the central-south of the Galápagos Archipelago, which are characterized by a particularly diverse combination of warm- and cool-water biota (Witman and Smith 2003) and show further spatio-temporal variation in communities within and between upwelling and non-upwelling areas (Banks 2003). Moreover, significant small-scale differences in benthic community structure between an upwelling and non-upwelling site of Floreana were described, but a change of the sessile community structure due to seasonality was evident exclusively for the non- upwelling site (Krutwa et al. unpublished).

Consequently, the main objective of the present study was to investigate natural benthic succession under upwelling and non-upwelling conditions in tropical rocky reefs off Floreana Island. The study was based on the following hypotheses: (1) succession proceeds through a consecutive replacement of species (2) the successional pattern differs between study sites due to different oceanographic conditions (upwelling and non-upwelling) (3) during succession, species richness increases initially, but declines later and (4) the convergence rate (defined as the time necessary for developing communities to converge to the surrounding natural community) (Pacheco et al. 2011) differs between the upwelling and the non-upwelling site, with the upwelling site having a higher convergence rate than the non-upwelling site. This was examined in order to determine a recovery rate for tropical rocky reef communities under upwelling and non- upwelling conditions and is, to our knowledge, the first comprehensive study on succession patterns in tropical subtidal rocky reef communities.

44 Chapter 2 Natural succession

Material and methods

Study sites The study was conducted off the island of Floreana located in the Galápagos Archipelago. We chose two different sites according to their oceanographic regime and accessibility. The first site, La Botella (LB), is located at the western coastline of Floreana (90º 29' 55.92'' W, 1º 17' 25.16'' S) and is exposed to strong upwelling events (Witman et al. 2010). The second site, named Tres Cuevitas (TC) is situated on the northeastern shore (90º 24' 30.26'' W, 1º 14' 6.45'' S) and represents a non-upwelling site with warmer waters and a well-mixed layer (Banks 2003). Temperature profiles of both sites underlining these site-specific abiotic differences are shown in Figure 2 and originated from a previous study by Krutwa et al. (under review).

Experimental design and sampling We investigated succession in the sessile benthic community by deploying settlement plates at 15 m depth at the two study sites in March 2009. In order to provide natural conditions for settlement and to be able to compare assemblages between experiments and the natural substrate we used natural lava substrate that was devoid of biota at the start of the experiment. The lava substrate was cut into square plates (25×25 cm and embedded in concrete (Figure 1) to keep the lava plates on the bottom. Since small-scale roughness can affect settlement, the substrate surfaces were categorized as either homogenously smoothed or furrowed. Both surface roughness types were treated separately with five replicates each. Lava plates were arranged randomly. Succession on the plates was monitored for two years until March 2011.

Plates were sampled by scuba diving after 12, 21, 30, 38, 45, 54 and 103 weeks. Percentage cover of the community was estimated by the point intercept method, which involved placing a 25×25 cm quadrat with 36 intersection points placed exactly on each lava plate. Algae and sessile invertebrates at each intersection were identified to the lowest taxonomic unit possible and counted. Additionally, the sessile community (algae and sessile invertebrates) was surveyed adjacent to the experimental lava plates after 103 weeks. Furthermore, taxa were assigned to functional groups.

45 Chapter 2 Natural succession

Figure 1. A) Experimental lava substrates at 15 m depth at the non-upwelling site, Tres Cuevitas. B) Red algae Schizymenia ecuadoreana at the upwelling site (La Botella) C) Hard coral Pavona clavus at the non-upwelling site (TC).

Data analysis Surface roughness did not have a significant effect on the percent cover of colonizing species (PERMANOVA test results,Table A1). Consequently, the data were pooled across substrate treatment for further analysis which resulted in ten replicate plates for each time period.

Univariate statistical analyses of community data were carried out with the program SigmaPlot 12.5. Differences in species richness S and evenness J were tested using one- way Repeated Measures Analysis of Variance (ANOVA) if data were homogeneous (Levene’s test) and normally (Shapiro-Wilk test) distributed. Otherwise data were analyzed with the Friedmann Repeated Measures-ANOVA. Tukey’s test of honestly significant difference (HSD) was used as post-hoc test. To compare the different communities by species composition, all communities were analyzed by Analyses of Similarity (ANOSIM) using Primer v6 (Clarke and Warwick 2006). Data were square root transformed in order to scale down the importance of highly abundant species.

46 Chapter 2 Natural succession

ANOSIMs were based on Bray-Curtis similarity indices. Similarity percentages (SIMPER) were used to determine the relative contribution of single taxa responsible for differences in species composition among treatments. To visualize changes between different assemblages during successional stages, the transformed data were subsequently analyzed using cluster analysis in combination with the similarity profile (SIMPROF) routine based on Bray-Curtis similarity matrices. Identified clusters as well as differences in community structure between natural vs. 103 weeks old assemblages were visualized using multi-dimensional scaling (MDS) plots.

Results

General pattern of species composition Overall, the epibiotic assemblages on lava plates between 12 and 103 weeks at the upwelling and non-upwelling sites (LB and TC, respectively) consisted of a total of 50 different taxa and functional groups (Table 1). We found 28 taxa of macrobenthic fauna, including ascidians (7 identified species, 1 unidentified), bryozoans (6 identified species, 1 unidentified), sponges (2 identified species, 2 unidentified), mollusks (3 species), hydrozoas (2 identified species, 1 unidentified) and polychaetes (2 identified species, 1 unidentified). Furthermore, we distinguished 8 algal functional groups (Steneck and Dethier, 1994) articulated calcareous algae (2 identified species), crustose algae (3 identified species), filamentous algae (1 identified species and 3 suborders green, red and brown filaments), foliose algae (3 species), corticated foliose algae (3 species), corticated macroalgae (1 identified species), microalgae (1 identified species) and leathery macrophytes (2 identified species). Two algae species remained unidentified. Red cyanobacteria were also found during the succession study.

47

Table 1. Mean (±SD) percentage cover of taxa/species found on lava settlement plates on 7 different weeks during succession in La Botella and Tres Cuevitas (12-103 weeks).

Succession at La Botella (LB) and Tres Cuevitas (TC) (in weeks) No. Taxa/species 12 21 30 38 45 54 103 LB TC LB TC LB TC LB TC LB TC LB TC LB TC 1 Aplidium solidum 0.3±0.9 0.3±0.9 0.3±0.9 2 Aplidium spp. 0,3±0.9 0.3±0.9 0.6±1.2 0.3±0.9 0.6±1.2 0.3±0.9 0.8±1.3 0.6±1.2 0.6±1.2 0.3±0.9 0.3±0.9 0.9±2.8 0.8±1.3 3 Ascidia spp. 0.8±1.3 0.8±1.3 0.3±0.9 0.3±0.9 0.3±0.9 0.3±0.9 4 Botryocladia spp. 0.3±0.9 5 Bryopsis spp. 0.3±0.9 0.3±0.9 0.3±0.9 0.3±0.9 0.3±0.9 6 Bugula cf. californica 0.6±1.2 0.3±0.9 0.3±0.9 0.3±0.9 0.6±1.2 7 Bugula neritina 0.6±1.8 0.6±1.2 0.3±0.9 1.4±2.0 8 Ciocalypta spp 0.3±0.9 1.4±1.5 48 9 Cleidochasma porcellanum 2.8±2.6 1.1±3.5 0.8±1.3 10 Codium spp. 0.3±0.9 11 Corallina spp. 0.8±1.3 12 Diatomea diatomea 24.4±21.3 0.9±1.3 0.6±1.2 1.1±1.9 0.8±1.9 1.7±2.7 2.2±3.2 1.4±2.7 0.6±1.2 13 Dictyota spp. 0.3±0.9 1.4±3.0 14 Didemnum perlucidum 0.6±1.2 15 Didemnum spp. 1.4±2.0 1.1±1.4 2.2±2.6 0.6±1.1 2.5±2.8 1.1±1.9 1.7±3.0 1.7±3.0 1.9±2.9 1.4±1.5 1.4±2.0 1.4±1.5 0.9±2.0 0.3±0.9 16 Eudistoma spp. 0.6±1.8 0.6±1.2 1.1±2.7 1.4±2.7 0.3±0.9 0.3±0.9 17 Gymnogongrus spp. 0.6±1.2 0.3±0.9 0.8±1.3 1.7±2.7 0.3±0.9 1.1±2.7 0.3±0.9 6.7±9.3 0.6±1.2 8.6±8.6 0.8±1.3 6.4±6.0 1.5±2.4 5.8±9.1 18 Haliclona spp. 1.1±1.9 1.4±2.4 1.4±2.0 1.9±1.3 0.3±0.9 1.9±2.6 19 Schizymenia ecuadoreana 0.8±1.9 2.2±2.9 3.7±4.6 20 Hildenbrandia spp. 10.8±7.9 2.8±1.3 13.6±8.8 2.5±1.6 11.9±9.4 2.5±2.4 11.1±10.1 2.3±2.6 16.1±8.8 2.8±2.6 13.3±5.2 1.9±1.9 14.2±9.7 4.7±6.3 21 Hipponix spp. 1.1±3.5 0.3±0.9 0.3±0.9 0.6±1.2 22 Hippoporina verrilli 1.1±1.4 0.8±1.3 0.8±1.3 1.1±1.4 2.5±0.9 0.3±0.9 0.6±1.2 0.3±0.9 0.3±0.9 0.3±0.9 0.6±1.2 6.2±17.5 23 Hypnea spp. 1.4±1.5 0.3±0.9 1.9±1.9 2.2±2.6 3.3±5.2 4.2±5.6 24 Isognomon recognitus 0.3±1.3 0.6±1.2 0.3±0.9 0.9±1.3 0.6±1.2 1.9±1.3 25 Jania spp. 0.3±0.9 1.7±1.4 0.6±1.2 2.8±1.3 1.9±2.9 1.1±1.4 3.9±4.8

Table 1. continuation…

Succession at La Botella (LB) and Tres Cuevitas (TC) (in weeks) No. Taxa/species 12 21 30 38 45 54 103 LB TC LB TC LB TC LB TC LB TC LB TC LB TC 26 Lichenopora intricata 1.9±1.9 0.6±1.2 0.3±0.9 0.3±0.9 0.3±0.9 27 Lithothamnium spp. 32.5±23.1 7.2±2.7 45.3±20.4 10.6±9.9 55.8±16.3 36.4±19.5 46.1±24.3 33.6±19.7 52.8±17.4 36.4±14.0 54.7±15.4 35.0±18.1 49.1±22.7 53.9±54.9 28 Megalomma mushaensis 0.3±0.9 29 Obelia dichotoma 0.3±0.9 1.1±1.9 30 Padina spp. 0.3±0.9 0.3±0.9 0.3±0.9 0.3±0.9 0.3±0.9 1.1±3.5 31 Pennaria disticha 1.4±2.0 32 Pocockiella spp. 1.4±1.5 1.7±1.9 2.5±2.8 0.3±0.9 3.9±4.8 5.6±5.6 1.4±1.5 0.8±1.3 33 Pterosiphonia spp. 0.6±1.2 0.3±0.9 34 Pyura cf. haustor 0.6±1.2 0.3±0.9 0.3±0.9 0.8±1.3 0.6±1.2 0.6±1.2 0.8±1.9 0.6±1.2 0.3±0.9 1.1±1.4 0.9±2.0 0.8±1.9

49 35 Rhynchozoon rostratum 0.8±1.9 0.3±0.9 3.6±2.6 0.6±1.2 4.7±4.2 1.7±1.9 1.9±2.6 1.1±1.4 3.6±4.5 1.9±2.3 1.7±1.4 1.1±1.4 2.5±2.6 36 Salmacina tribranchiata 0.3±0.9 2.2±1.2 1.4±1.5 1.9±1.3 1.9±1.3 1.7±1.4 1.4±2.0 2.5±0.9 1.9±1.9 2.2±1.8 1.4±1.5 2.2±1.8 1.5±1.5 2.2±2.6 37 Serpulorbis margaritaceus 0.3±0.9 0.3±0.9 0.3±0.9 3.1±6.7 1.1±1.4 0.3±0.9 2.5±2.8 38 Ulva spp. 1.7±2.7 46.9±28.5 1.7±1.9 35.8±21.6 5.8±8.0 31.7±20.0 11.4±18.2 32.8±22.2 2.8±6.1 18.9±17.8 1.1±1.9 1.7±3.0 8.0±8.9 16.4±15.1 39 Filamentous brown algae 1.7±4.4 12.2±12.6 3.1±7.9 3.1±5.9 0.8±2.6 3.1±4.2 40 Filamentous green algae 6.4±19.3 23.6±33.0 5.3±14.8 24.7±30.5 3.1±4.2 5.3±15.7 8.3±8.4 0.6±1.8 5.6±10.1 4.4±6.8 8.9±9.0 23.3±25.7 0.9±2.0 16.4±16.7 41 Filamentous red algae 11.9±22.9 6.1±5.2 7.2±10.2 6.4±7.4 3.3±7.8 3.1±5.1 5.8±14.8 0.8±1.9 3.3±5.8 3.1±3.8 3.9±5.1 9.2±13.2 4.6±9.2 15.6±20.1 42 Orange sponge 0.3±0.9 0.3±0.9 0.3±0.9 0.3±0.9 0.6±1.2 43 White sponge 0.3±0.9 44 Polychaete tubeworm 1.4±1.5 0.3±0.9 1.1±1.4 0.3±0.9 1.1±1.4 0.3±0.9 0.9±1.3 0.6±1.2 0.9±1.3 0.3±0.9 0.6±1.2 45 Red cyanobacteria 1.4±4.4 0.3±0.9 46 Unidentified ascidia 0.3±0.9 47 Unidentified brown algae 0.3±0.9 0.3±0.8 0.3±0.9 48 Unidentified bryozoan 0.3±0.9 0.6±1.2 0.3±0.9 49 Unidentified hydroid 0.3±0.9 2.5±2.8 0.8±1.9 1.4±3.0 0.6±1.2 0.6±1.2 0.3±0.9 50 Unidentified red algae 0.8±1.9 0.3±0.9 0.3±0.9 1.9±4.5 0.3±0.9 0.6±1.8 1.7±1.9 0.6±1.9 1.1±2.3

Chapter 2 Natural succession

Succession patterns at study sites The epibiotic assemblage at the upwelling site (LB) comprised 17 species/taxa after 12 weeks, with the crustose algae Lithothamnium spp. as the most dominant, followed by the microalgae Diatomea diatomea (Table 1, Figure 2). After 21 weeks, D. diatomea decreased drastically and crustose algae (including Lithothamnium spp. and Hildenbrandia spp.) as well as filamentous algae became the most abundant groups in the community (Table 1, Figure 2, Table 2). Filamentous algae again decreased after 30 weeks (Table 1, Figure 2), but after that community composition remained the same (Table 2). In the adjacent area of the experimental lava plates, crustose algae clearly dominated (> 70 %) the epibiotic community (Figure 3).

The assemblage at the non-upwelling site (TC) consisted of 21 species/taxa after 12 weeks with the foliose algae Ulva spp. and green filamentous algae being the most abundant species and functional group, respectively (Table 1, Figure 2). There was a pronounced change in the composition of the developing community after 30 weeks (Table 2), mainly due to a large decrease in the percent cover of filamentous algae and a drastic increase of Lithothamnium spp. (Figure 2, Table 2). Community composition showed little change until after 103 weeks, mainly due to the increase of Ulva spp. as well as of Lithothamnium spp., which dominated the assemblage, and the decrease of filamentous algae and the corticated foliose algae Gymnogongrus spp. (Table 2). After 103 weeks, monitoring of the adjacent area of the lava plates indicated that the sessile benthic community was mainly comprised of four functional groups (≥ 20 %, crustose, foliose, corticated foliose algae and hard corals, Figure 3).

There were either significant changes in species richness over the two year duration of the experiment (Table 3, Figure 6), whereas evenness changed significantly at the non-upwelling site TC. Tukey’s test revealed significant differences in evenness between weeks 45 and 103 and weeks 12 and 103 (Table 3).

50 Chapter 2 Natural succession

Crustose algae Filamentous algae Foliose algae Microalgae Micro-omnivores Filter-feeders Corticated foliose algae 80 La Botella 15 m 28 70 26 60 50 24

40 22 30 20 20 18 10 0 16

80 Tres Cuevitas 15 m 28

Cover (%) 70 26 60 Temperature (ºC) 50 24

40 22 30 20 20 10 18 0 16 12 21 30 38 45 54 103 Successional stage (weeks) Figure 2. Changes in cover of the most abundant functional groups (reaching > 5%) during succession at A) La Botella and B) Tres Cuevitas. Values are means ± SE, n=10. Temperature profile is shown as grey shaded background.

80 Crustose algae Filamentous algae 70 Foliose algae Corticated foliose algae 60 Hard coral 50 40

Cover (%) 30 20 10 0 LB TC Study sites Figure 3. Percent cover (±SE) of most abundant functional groups (reaching > 5 %) surveyed in the adjacent area of succession experiments on March 2011 (successional stage: 103 weeks).

Comparison of community assembly in upwelling and non-upwelling conditions Comparison of succession on lava plates at three months (12 weeks), one year (54 weeks) and two years (103 weeks) indicated that the communities at the upwelling (LB) and non-upwelling site (TC) were significantly different (Figure 4, Table 2). After 12

51 Chapter 2 Natural succession weeks, assemblages showed a dissimilarity of more than 70 %, mainly due to Ulva and green filaments that dominated the community at TC while the community at LB was dominated by Diatomea and Lithothamnium (Table 2). Dissimilarity decreased after 54 weeks to 53 %, when differences were caused by more abundant filamentous and corticated foliose algae at TC as well as by the presence of the bivalve Isognomon recognitus, whereas crustose algae (Lithothamnium and Hildenbrandia) were the most abundant groups at LB (Table 2). After 103 weeks, significant differences between both sites were caused by an increase of green and red filaments as well as Ulva, a decrease of crustose algae and the absence of the red algae Schizymenia ecuadoreana at the non- upwelling site TC (Table 2).

Transform: Square root Resemblance: S17 Bray Curtis similarity 2D Stress: 0,1 site 103 LB TC 103 Similarity 38 45 30 60

30 38 21 21 45 12

54 54

12

Figure 4. Non-metric multi-dimensional scaling (nMDS) plot showing differences in community structure between successional stages of different ages (12-103 weeks) and sites (LB=La Botella and TC=Tres Cuevitas). Assemblage age is given as number of weeks. Superimposed clusters (line) identified by sequence of SIMPROF tests (p<0.05) on dendrograms at similarity levels of 60 %.

52 Chapter 2 Natural succession

The greatest difference in community composition between sites occurred after 12 weeks while the smallest difference occurred after 103 weeks (Figure 4). The developing community differed slightly after two years of succession from the surrounding natural community at the upwelling site LB, whereas at the non-upwelling site TC communities were very distant from each other (Figure 5).

Transform: Square root Resemblance: S17 Bray Curtis similarity natural community 2D Stress: 0 site LB TC Similarity 75

natural community

103weeks community

103weeks community

Figure 5. Non-metric multi-dimensional scaling (nMDS) plot showing differences in community structure between the surrounding natural community and the 103 weeks old community and sites (LB=La Botella and TC=Tres Cuevitas). Superimposed clusters (line) identified by sequence of SIMPROF tests (p<0.05) on dendrograms at similarity levels of 75 %.

53

Table 2. Analyses of similarity (ANOSIM) and similarity percentages (SIMPER) testing the succession Natural effects of successional stages (in weeks) at each site and 2 Chapter between sites for 12-, 30-, 54- and 103-week-old assemblages.

Succession at LB ANOSIM (overall) Global R=0.184, p=0.001 Successional stages 12→21 21→30 30→38 38→45 45→54 54→103 ANOSIM R=0.429, p=0.001 n.s. n.s. n.s. n.s. n.s. SIMPER Dissimilarity 56.4% 15.8%-Diatomea 10.8%+Brown filam. 9.8%-Red filam. 9.8%+Lithothamnium 7%+Hildenbrandia Succession at TC ANOSIM (overall) Global R=0.356, p=0.001 ANOSIM n.s. R=0.276, p=0.001 n.s. n.s. n.s. R=0.316, p=0.001 SIMPER Dissimilarity 51.7% Dissimilarity 52.6% 16.1% -Green filam. 10.3%+Ulva

54 11.8%+Lithothamnium 8.9%+Lithothamnium 9.5%-Ulva 8.6%-Green filam. 6.4%-Red filam. 8.3%-Red filam. 4.5%+Hippoporina 6.3%-Gymnogongrus 4.3%-Unid. hydroid 4.2%+Jania 4.1%a Isognomon Between LB and TC ANOSIM (overall) Global R=0.465, p=0.001 Sites LB12weeks↔TC12weeks LB54weeks↔TC54weeks LB103weeks↔TC103weeks ANOSIM R=0.748, p=0.001% R=0.479, p=0.001% R=0.43, p=0.001 SIMPER Dissimilarity 70.8% Dissimilarity 53.6% Dissimilarity 54.9% 17.3%+Ulva 9.6%-Lithothamnium 10.8%+Green filam. 12.1%-Diatomea 9.6%-Hildenbrandia 8.9%+Red filam. 11.4%+Green filam. 9.5%+Green filam. 8.5%+Ulva 9.5%-Lithothamnium 7.1%+Red filam. 8.1%-Hildenbrandia 6.7%+Gymnogongrus 7.8%-Lithothamnium 4.2%p Isognomon 5.2%a Schizymenia 4.1%-Diatomea Global analysis results of ANOSIM (R, p) testing for both individual and paired treatment differences are also given. Results of SIMPER analysis are given as percent dissimilarity for each significantly different treatment pair, followed by the percent contribution of each single species/taxon to the difference. The table shows all species/taxa that contributed to > 50 % of species composition between treatments. Increased or decreased abundance and absence or presence of each species/taxon with respect to succession time or site (LB→TC) are symbolized with +/- and a/p, respectively. n.s.=not significant. Chapter 2 Natural succession

There were no significant differences in average species richness at the non- upwelling site TC after 12, 54 and 103 weeks of succession, whereas evenness was significantly higher at the upwelling site LB after 12 weeks (Figure 6, Table 3). After 54 and 103 weeks there was a trend toward greater evenness at TC than at LB although this trend was not significant (Figure 6, Table 3).

Table 3. Overview of different analyses comparing univariate diversity measurements, average species richness (S) and evenness (J') using analysis of variance (ANOVA, F) or Friedmann Repeated Measures ANOVA (Χ2) for differences between assemblages of different successional stages at each site (factor: age) and between sites at 12, 54 and 103 weeks (factor: site).

Analyses df Factor S J´ Succession at 6 Age La Botella n.s. n.s. Tres Cuevitas n.s. Χ2=15.04, p<0.05 45↔103weeks 12↔103weeks Different sites 1 Site 12 weeks n.s. F=6.62, p<0.05 54 weeks n.s. n.s. 103 weeks n.s. n.s.

16 LB TC

12

S 8

4

0

0.8

0.6 J' 0.4

0.2

0 12 21 30 38 45 54 103

Successional stage (weeks) Figure 6. Changes in average species richness (S) and evenness (J') during succession at both sites.

55 Chapter 2 Natural succession

Discussion

Differences in succession patterns at both study sites Succession preceded differently at the two study sites. Three groups, crustose algae, microalgae (D. diatomea) and filamentous algae dominated at the upwelling site LB after three months. Nine weeks later, D. diatomea was widely replaced by the increasing cover of the crustose algae Lithothamnium spp. and Hildenbrandia spp. These findings agree with observations by Cifuentes et al. (2010) in the highly productive Humboldt Current Upwelling system, where the structure of fouling communities differed in the initial and intermediate successional stage due to variability in recruitment peaks of settlers but once a dominant species was present, competitive exclusion quickly caused a homogenization of the community towards a single stable state. At the upwelling site LB, Lithothamnium spp. dominated the epibenthic community after 21 weeks and the assemblage structure remained stable during the following successional stages. Vermeij et al. (2011) found that crustose coralline algae are able to reduce macroalgae growths rates (e.g. Ulva fasciata) and recruitment success. In the present study, foliose algae cover was very low at the upwelling site LB. At the non-upwelling site TC, in contrast, foliose and filamentous algae were more abundant initially and were replaced by crustose algae during succession and D. diatomea was negligibly abundant. Further, the increase of the bryozoan Hippoporina spp. and the decrease of an unidentified hydroid affected the assemblage structure after 30 weeks. Even during late succession (between 54 and 103 weeks) the epibiotic assemblages changed significantly. Hence, our study results show that the trajectory of the succession is more predictable and convergent at the upwelling site LB (“canalized succession”) whereas, a more variable and divergent settlement pattern was observed for the non-upwelling site TC (“contingent succession” i.e. Berlow 1997). This variable, contingent succession may be also a response to a stronger seasonality at this site, which was observed in a previous study by the authors. At TC the sessile community showed seasonal differences, while it remained unchanged at LB throughout the year suggesting a suppression of seasonality by strong upwelling (Krutwa et al. unpublished). These findings are similar to those of Pacheco et al. (2011) who found that that seasonality had no effects on succession in reported for a highly productive coastal upwelling area.

Generally, the developing assemblages under upwelling (LB) and non-upwelling (TC) conditions differed significantly from each other (Figure 4). Comparing the

56 Chapter 2 Natural succession successional stages after three months, one year and two years between both sites, differences were mainly due to higher cover of Lithothamnium spp. and to lower cover of filamentous algae and Ulva spp. at LB, to lower cover of Lithothamnium spp and to higher cover of filamentous algae and Ulva spp. at the non-upwelling site TC. Furthermore, the sessile bivalve Isognomon spp. was only found at TC, whereas the red algae S. ecuadorena grew exclusively on lava plates at LB. This critically endangered alga (Miller et al. 2007) is endemic to the Galápagos Archipelago and was reported before at only three sites, namely Floreana, Isabela and Fernandina (Miller et al. 2007). Thus, here we add a fourth site, even though this species disappeared during the warm season. These small-scale differences between both sites were also found for the natural surrounding community (Krutwa et al. unpublished). It is known that upwelling influences the structure of subtidal benthic communities by affecting recruitment (Roughgarden et al. 1988, Menge et al. 2003, 2004, Witman et al. 2010), growth of algae (Bustamante et al. 1995) and the abundance of epifaunal invertebrates (Branch and Griffith 1988). Interestingly, the pattern found in our study, with a crustose algal dominated community at the upwelling site LB and a more diverse community (including foliose, crustose, corticated, foliose algae and hard corals) with no single dominating taxa at TC, occurred vice versa at intertidal communities of South African coast under different upwelling regimes (Bustamante et al. 1995). There, the upwelling area was dominated by filamentous, foliose and corticated algae, while crustose corallines and non-coralline turfs were the most abundant groups at the non-upwelling area. Bustamante et al. (1995) explained the low abundance of foliose algae at the non- upwelling site by the lower nutrient loads and the high fish grazing pressure here. However, the authors were not able to explain the high standing stock of foliose algae at the upwelling site, where both nutrient input and grazing pressure was high (Bustamante et al. 1995). Overall, upwelling changes the intensity of species interactions (Sanford 1999, Menge et al. 2003, 2004, Witman et al 2010 for predation), and hence, future studies should investigate the effect of grazing pressure at TC and LB.

Species richness and evenness Sousa (2001) described an increase in species richness at the beginning of the succession trajectory, which declines later with the monopolization of the substratum by one species. In this study, we did not sample the developing communities immediately after the onset of the experiment but instead followed he community assembly from 3

57 Chapter 2 Natural succession months to 2 years. During this period species richness between successional stages did not significantly change at both sites. It is possible that a large part of the early succession process and increase in species richness (Fricke et al. 2011) had already been completed within the first 3 months. The diversity of the vagile fauna within the developing assemblages was not recorded in our study, which may have influenced the succession path at both sites. For example, in a temperate rocky reef Antoniadou et al. (2011) found an increase of motile benthic colonizers during succession progress, which seemed to go along with increasing habitat complexity through the development of the sessile community on the substratum. However, Underwood and Chapman (2006) suggested a community development that is not caused by the increase in taxa richness but by the replacement of taxa. Differences in evenness at the non-upwelling site TC could be explained by the variable settlement pattern described above (Berlow 1997).

Species richness was significantly higher at the non-upwelling site after 3 months and at one year of succession, but these differences disappeared after two years. These findings were confirmed in a former study by Krutwa et al. (unpublished), who found significant differences in evenness, whereas in the present study no differences in evenness were evident between sites after one year. Here, the differences in oceanographic conditions (upwelling vs. non-upwelling) do not seem to drive differences in diversity at both study sites after one and two years of sessile community development, although it is known that upwelling depending on its intensity can also have different effects on species richness (Santelices et al. 2009). When strong and permanent upwelling occurs in tropical warm-water areas, macroalgal species richness decreases, while weak and seasonal upwelling can increase macroalgal diversity due to their adaptability to a broader range of oceanographic conditions and hence diversity of different thermally adapted species may increase (Santelices et al. 2009).

Convergence to natural surrounding community After two years of succession community structure at the upwelling site was similar to the established community at the study site (Figure 5) Further, the percent cover of functional groups of the natural communities resembled that of the developing communities on lava plates (Figure 2 and 3) with crustose algae dominating the assemblages. This seems due to the fast growth and extension rates of crustose corallines (10.8-27.6 mm per year), as reported by Adey and Vassar (1975) for the

58 Chapter 2 Natural succession

Virgin Islands. This is relatively fast when compared to growth rates of scleractinian corals such as Pavona gigantea, P. clavus and Porites lobata found at the non- upwelling site TC. Glynn and Wellington, (1983) reported growth rates between 6.8 and 17.5 mm per year for those coral species in the Galápagos Archipelago. The natural sessile community at the TC site is characterized by a high cover of hard corals, mainly P. gigantea (>23 % coverage), whereas those corals were still absent from epibiotic assemblages on the experimental plates after two years of succession. In general, recovery times of coral reef dominated communities are estimated to range from 10 to 30 years (Hughes 1994, Connell et al. 1997, Done 1999), whereas faster recovery times are reported for communities in upwelling areas (Witman and Smith 2003, Pacheco et al. 2011). No recruitment of corals occurred during our study, which may be due to the low recruitment rates of scleractinian coral (Kojis and Quinn 2001).

Conclusions and Outlook

In this study, the successional development of benthic communities was investigated over a two year period at an upwelling and non-upwelling site off the island of Floreana, Gálapagos. The sites were 17 km apart and the succession experiments used lava plates as natural substratum. Results show a more canalized succession at the upwelling site, whereas the non-upwelling site was characterized by a more random pattern (Berlow 1997). The different patterns observed suggest high variability of ecological processes within a single biogeographic region (Edgar et al. 2004). This result is similar to that of Witman et al. 2010, who found that predation varied significantly along an upwelling gradient in the same region of the Galápagos Islands. This variation may also partially explain the coexistence of communities of different successional stages (Platt and Connell 2003, Cifuentes et al. 2010).

As the main focus of this study was to examine differences in succession pathways between an upwelling and a non-upwelling site over the long term no sampling was conducted during the first three months. Thus, information about possible differences in pioneer species, which settled first and may facilitate succession, is lacking at both sites. Furthermore, the timing of the start of succession (seasonality) may influence the successional pathway (Underwood and Chapman 2006). At the upwelling site LB and the non-upwelling site TC, the colonized vs. uncolonized space differed after three

59 Chapter 2 Natural succession months depending on the time of exposure and start of succession, with higher percent cover of epibiota during the cold season (unpublished data). However, as mentioned before, assemblage structure might differ at early and intermediate succession, but develop during late successional stages to a stable single state (Cifuentes et al. 2010), although recovery might be faster depending on the season (Antoniadou et al. 2011).

In terms of the recovery of the communities from disturbances creating space on the rocky substrate, the upwelling site seemed to recover relatively faster as the developing community structure was more similar to the natural community around after two years. These findings are similar to those by Witman and Smith (2003), who found a rapid community change after one year for an upwelling site in the Galápagos Archipelago suggesting a quick recovery for certain groups. In contrast, recovery needs more time at the non-upwelling site because of slowly growing hard corals, which form an important part of this community. Yet, our findings suggest that colonization and further development of the communities is still occurring at the two sites. Comparisons between recovery rates of subtidal hard bottom communities in other areas are difficult to make due to differences in climate regions, habitats and experimental approaches. However, few studies suggest a relatively slow pace of recovery of more than one year during cold upwelling conditions (Pacheco et al. 2011) and about two years in temperate reefs (Antoniadou et al. 2010). Moreover, joint effects of herbivores and algal species richness may increase the recovery rate (Aquilino and Stachowicz 2012). Consequently, further experiments that include the potential effects of grazers and predators on succession should be conducted to fully understand the dynamics of subtidal succession in the Galápagos Islands.

Acknowledgements

The authors acknowledge the Charles Darwin Foundation and the Galápagos National Park Service. AK thanks the German Academic Exchange Service (DAAD) for scholarship. Many thanks go to Roberto Pepolas, Julio Delgado, Jerson Moreno, Janaí Yépez and other volunteers for indispensable help in the field.

60 Chapter 2 Natural succession

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Appendix

Table A1. PERMANOVA tests on community structure on lava plates of two surface roughness types (S–smoothed, F–furrowed); LB=La Botella, TC=Tres Cuevitas.

Source df MS Pseudo-F P(perm) Location 1 40050 30.299 0.001 Surface roughness 1 4116.1 3.114 0.003 Location x surface roughness 1 682.54 0.516 0.85 Residual 135 1321.8

Pair-wise test t P(perm) LB: S-L 1.245 0.149 TC: S-L 1.435 0.057

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68 Chapter 3 Grazing effects

3 Grazing effects on tropical rocky reef communities exposed to upwelling and non-upwelling conditions in Galápagos (Ecuador)

Annika Krutwa, Diego J. Ruiz, Matthias Wolff

Leibniz Center for Tropical Marine Ecology (ZMT) GmbH, Fahrenheitstrasse 6, 28359 Bremen, Germany ______

Abstract

The impact of grazers on benthic communities is of great interest since their abundances are often modified by anthropogenic impacts (e.g. fishing pressure, eutrophication) as well as by natural- and human-induced changes in climate patterns (ENSO, global warming). Unlike the well-studied coral reefs, the effects of grazer pressure on tropical subtidal rocky reef communities have only rarely been studied. This one-year study investigated the effects of grazers during the benthic succession at two sites, one exposed to upwelling and another one to non-upwelling conditions, off Floreana Island, located in the Galápagos Marine Reserve. The experiment consisted of in situ deployments of caged and uncaged natural lava plates at a depth of 15 m, which were surveyed every 2 to 3 months. Grazing fish and macroinvertebrates were quantified throughout the study by transect sampling. Our findings point to strong impacts of herbivorous fish and macroinvertebrate grazer on benthic community composition (top- down) at the non-upwelling sites, whereas effects were less conspicuous at the upwelling site despite significantly higher grazer abundances (bottom-up). At both sites, differences between caged and uncaged plates were due to less contribution of anemones and an increase of Ulva spp. to species composition in the grazer exclusion plots. Results suggest that small-scale (< 17 km) differences in oceanographic conditions within the same biogeographic region greatly influence the ecological interactions with bottom-up effects dominating at upwelling and top-down effects at non-upwelling sites.

Keywords: benthic communities, bottom-up, exclusion experiments, Galápagos, grazing, subtidal, top-down, tropical rocky reef, upwelling vs. non-upwelling ______

69 Chapter 3 Grazing effects

Introduction

The effects of grazing (top-down) and the delivery of nutrients (bottom-up) on marine communities are of great interest as changes can cause dramatic impacts on the entire marine system. Top-down effects can be modified due to overfishing and introduction of alien species (Jackson et al. 2001, Duffy 2003, Castilla et al. 2005, Estes et al. 2011). For example, in the Caribbean declines of grazers (herbivorous fish and sea urchins) caused phase shifts from coral- to algal-dominated communities (Hughes 1994). Bottom-up effects can be altered due to changes in nutrients supply (i.e. eutrophication, Smith et al. 1999) and large-scale environmental disturbances such as the El Niño Southern Oscillation (ENSO) (Barber and Chavez 1983, Chavez et al. 1999, Edgar et al. 2009) and the anthropogenic induced climate change (Post et al. 2009). Further, the combination of these factors can lead to an elevation of an extinction risk for marine species and a reduction of the resilience of an ecosystem (Hughes et al. 2003, Edgar et al. 2009).

Burkepile and Hay (2006) suggested that the impact of grazers on the abundance and type of algal functional groups varies with latitude. In the tropics, herbivores had great effects by generally reducing algal biomass, whereas at higher latitudes, effects varied depending on the productivity. At sites of higher productivity grazing had little to no effect on species composition, but, in contrast, at sites of low productivity they had strong top-down effects on the diversity of primary producers. For the tropics, Burkepile and Hay (2006) and others (Diaz-Pulido and McCook 2003, Boyer et al. 2004) also showed that grazers can compensate for higher nutrient levels by facilitating grazing-resistant species of algae and reducing total algal biomass. This suggests that top-down effects are stronger than bottom-up effects and is coherent with other studies indicating strong grazing impacts on tropical marine systems (Menge and Lubchenco 1981, Burkepile and Hay 2008).

The impact of herbivory was widely studied for coral reef communities (e.g. Carpenter 1986, Hughes et al. 1987, Hixon and Brostoff 1996, Mumby 2006, Hughes et al. 2007), but actual information on grazer impacts on tropical shallow rocky reef communities is rare (Irving and Witman 2009, Witman et al. 2010, Brandt et al. 2012). Further, there is no knowledge available about grazing effects in contrasting

70 Chapter 3 Grazing effects oceanographic environments (i.e. upwelling vs. non-upwelling). For the tropics, a recent study on Galápagos rocky intertidal communities (Vinueza et al. 2013) showed that the relative importance of bottom-up and top-down effects varied with oceanographic regime and climate variability.

The Galápagos Marine Reserve (GMR) was established in 1998 by the Ecuadorian government, and is with an area of 133.000 km2 the sixth largest Marine Protected Area in the world. The Reserve is located in the Eastern Tropical Pacific about 1000 km west of Ecuador’s coast and lies in a complex transition zone between tropical, subtropical, and upwelling waters (Schaeffer et al. 2008). Surface waters from the cold Humboldt Current (20-22°C) arrive from the south influencing the southern islands, while waters of the warm North Equatorial Countercurrent (26-29°C) affect the northern islands (Kessler 2006). Both currents change in relative intensity and position with the location of the Intertropical Convergence Zone and add to the effect of the westward flowing South Equatorial Current (Houvenaghel 1984). This current causes a strong counter flow, named the Equatorial Undercurrent, which flows from west to east and collides with the western side of the archipelago provoking major topographic upwelling (Chavez and Brusca 1991, Houvenaghel 1984). Branches of the Equatorial Undercurrent running through the archipelago are responsible for upwelling at a smaller scale, e.g. the southwest of Floreana Island and the northeast of Santa Cruz Island (Schaeffer et al. 2008) and further, topographically induced upwelling occurs in the form of island wakes (Feldman 1986, Houvenaghel 1978) and internal waves (Witman and Smith 2003).

Previous studies on Galápagos subtidal rocky reef communities at an upwelling and a non-upwelling site and their succession processes showed significant differences in community structure and succession patterns between both sites (Krutwa et al. unpublished), but the influence of grazers, such as herbivorous fish and macroinvertebrate grazer has not yet been investigated. In the present study, grazing exclusion experiments were used to study grazing pressure on subtidal rocky reef communities off Floreana Island, located in the central-south region of the Archipelago, which are characterized by a diverse combination of warm- and cool-water biota (Witman and Smith 2003) varying within and between upwelling and non-upwelling areas (Banks 2003).

71 Chapter 3 Grazing effects

Due to significant differences in the community structure of subtidal rocky reefs between the upwelling and non-upwelling site found in previous studies (Krutwa et al. unpublished) we hypothesize that grazing effects may also differ between both sites. Therefore, our objectives were: 1) to describe differences in community structure under natural and experimentally excluded herbivory at an upwelling and a non-upwelling site off Floreana, 2) to determine the major functional algal and sessile invertebrate groups occurring during grazed and ungrazed succession at both study sites, 3) to determine species and/or taxonomical groups contributing to observed differences and 4) to examine differences in diversity (species richness S and evenness J') of epibiotic communities among grazed and ungrazed treatments and between both sites. Further, fish and macroinvertebrate grazer surveys were conducted to determine abundances and species composition of potential herbivores at both sites.

Material and methods

Study site and experimental setup The study was conducted at two different sites off the island of Floreana (Figure 1). The first site, La Botella (LB), is situated at the western coastline of the island (90º 29' 55.92'' W, 1º 17' 25.16'' S) and is characterized by strong upwelling events (Witman et al. 2010). The second site, Tres Cuevitas (TC) is located on the northeastern shore (90º 24' 30.26'' W, 1º 14' 6.45'' S) and embodies a non-upwelling site with warmer waters and a well-mixed layer (Banks 2003).

To examine the effects of grazing on the succession of the sessile community, we exposed 2 different treatments: open and closed (caged) settlement plates at 15 m water depth at both study sites from March 2009 to March 2011. We used natural lava substratum, which was completely clean of biota in order to provide natural conditions for settlement (McGuiness 1989). The lava substrate were cut into square plates (25×25 cm) and embedded in concrete to keep the plates at the bottom of the reef. Exclusion cages were constructed with plastic mesh (25×25×12 cm) with a mesh size of 3.5 cm and cable ties. Cage controls were not used, since previous studies had shown no or minor cage effects on light availability, water movement and sedimentation rates (Hixon and Brostoff 1996, Miller et al. 1999, Smith et al. 2001). Settlement plates were placed

72 Chapter 3 Grazing effects in the cages and closed with cable ties. At each site, open (n=2x5) and closed (n=2x5) experimental plates were arranged randomly and cages were cleaned on every field trip.

90º30’ S 90º25’ S 90º20’ S

FLOREANA ISLAND GALAPAGOS S ’ 100 m N 1º 10 50 m 1

S 20 m ’ 1º15

2

50 m m 50 50

20 m 20 20 m 20 Island S ’ Study sites

1º20 Iso-bathimetry

100 m m 100 100 S ’ 1º25

1 Tres Cuevitas 2 La Botella

20 m 20 m

20 m

Figure 1. Study sites: Tres Cuevitas (TC) and La Botella (LB).

Data sampling Experimental treatments and grazer abundances were surveyed by scuba diving after 0, 12, 21, 30, 38, 45, 54 and 103 weeks. The percentage cover of the community was estimated by using a 25×25 cm quadrant with 36 intersection points placed exactly on each settlement plate. Mobile macroinvertebrate grazer abundance data were collected within a 1 m corridor at both sides every 25 m along a 50 m transect. Reef fish species and abundances were registered along a 5 m2 corridor on both sides of the 50 m transect, resulting in a total of 500 m2 area coverage per transect and of 8 transects in total.

Species were identified to the lowest taxonomic level possible and taxa were assigned to functional groups. Alga taxa were grouped based on Steneck and Dethier

73 Chapter 3 Grazing effects

(1994) and Phillips et al (1997) and the sessile fauna on their commonly known feeding habits. Fish were classified into herbivorous and non-herbivorous groups, including facultative herbivores (Froese and Paula 2014, Human and DeLoach 2003).

Data analysis Univariate and multivariate statistical analyses of community data were conducted using SigmaPlot 12.5 and Primer v6. Abundance data of herbivorous fish and macroinvertebrate grazer of the 8 transects were pooled. If data were homogeneous (Levene’s test) and normally (Shapiro-Wilk test) distributed, differences in abundances between sites as well as in species richness (S) and evenness (J') between sites and treatments were tested using one-way Analysis of Variance (ANOVA). Otherwise data were analyzed with the Kruskal-Wallis test and as post-hoc test Tukey’s test of honestly significant difference (HSD) was used. In order to compare the different assemblages by species composition, all communities were analyzed by Analyses of Similarity (ANOSIM). Data were square root transformed in order to scale down the importance of highly abundant species and ANOSIMs were based on Bray-Curtis similarity indices. Similarity percentages (SIMPER) were used to determine the relative contribution of single taxa responsible for differences in species composition among treatments. To visualize differences between sites and cage effects during successional stages, the transformed data were subsequently analyzed using cluster analysis in combination with the similarity profile (SIMPROF) routine based on Bray-Curtis similarity matrices. Identified clusters of experimental treatments were visualized using multi-dimensional scaling (MDS) plots.

Results

Succession of functional groups On the open and closed lava plates, the different epibiotic assemblages grown between 12 and 103 weeks at the upwelling site LB and the non-upwelling sites TC consisted of a total of 63 different taxa and taxonomical groups (Table A1). We found 33 taxa of macrobenthic fauna, which were differentiated into 5 functional groups (filter-feeders, micro-omnivores, micro-carnivores, deposit-feeder and carnivores with photosynthetic symbionts). Furthermore, we distinguished the following 8 functional algae groups (Steneck and Dethier 1994, Phillips et al 1997): articulated calcareous

74 Chapter 3 Grazing effects algae, crustose algae, filamentous algae, foliose algae, corticated foliose algae, corticated terete algae, microalgae and leathery macrophytes, comprising 29 taxa. Red cyanobacteria were also present during the succession.

Assemblages of caged plots differed greatly (less than 60 % similarity) from those of open plots at TC, whereas caged and open plots at LB show a similarity of 60 % (Figure 2). The microalgae Diatomea diatomea was found only in the open plot at LB after 12 weeks. Apart from that, closed and open plots at LB show a similar composition of the community comprised of five major functional groups (>5 % coverage) with crustose algae as the dominant group covering between 43 and 69 %. At TC, foliose and filamentous algae dominated together with crustose algae the assemblage. There, the community of the closed plots consists of 8 major functional groups including the exclusively occurrence of cyanobacteria after week 21, micro- omnivores after week 12 and of corticated terete algae after weeks 38 and 45 (Figure 3).

Figure 2. Non-metric multi dimensional scaling (nMDS) showing differences in community structure of different old epibiotic assemblages of open and closed treatments at LB and TC. Assemblage age is given as number of weeks. Superimposed clusters (line) identified by sequence of SIMPROF tests (p<0.05) on dendrograms at similarity levels of 60 % and 75 %.

ANOSIMs (Table 1) show that differences between closed and open plots at LB were mainly due to the occurrence of an anemone in the open plot, which could not be identified, as well as microalgae and filamentous algae. At TC, the grazer exclusion

75 Chapter 3 Grazing effects caused a decrease in the cover of the same unidentified anemone and an increase of Ulva spp.. Assemblages of closed plots differ significantly between sites as well as assemblages of open plots (Table 1).

La Botella-closed Tres Cuevitas-closed 100

80

60

40

20

0

La Botella-open Tres Cuevitas-open

Cover (%) 100

Micro-omnivores 80 Filter-feeders Cyanobacteria 60 Corticated terete algae Corticated foliose algae 40 Microalgae Foliose algae 20 Filamentous algae Crustose algae 0 12 21 30 38 45 54 103 12 21 30 38 45 54 103 Successional stage (weeks) Figure 3. Succession of various functional groups (>5 % cover) in open and closed treatment at each site (LB and TC) over 103 weeks.

Species richness and evenness Grazer exclusion caused higher species richness at both sites (Figure 4), but the differences found were statistically significant only at LB (ANOVA: F1,12=7.6, p=0.017). Open plot species richness at TC exceeded that at LB (ANOVA: F1,12=10.0, p=0.008), and closed plot evenness was higher at TC (ANOVA: F1,12=17.9, p=0.001).

76 Chapter 3 Grazing effects

open closed 30

20 S

10

0

0.8

0.6

J' 0.4

0.2

0 LB TC Figure 4. Differences in species richness (S) and evenness (J’) of different epibiotic communities, LB and TC, exposed to open and closed treatments. Data showing mean values ± SD.

Herbivorous fish and macroinvertebrate grazer abundance During the fish surveys, a total of 43 (LB) and 39 (TC) species were observed. Herbivorous fish were represented by 9 and 8 species, respectively (Table 2). Herbivorous fish abundance was significantly higher at LB (0.8±0.1 ind. m-2) than at TC (0.3±0.1 ind. m-2). The razor surgeonfish Prionurus laticlavius accounted for 74.6 % at LB and 60.3 % at TC of all observed herbivorous fishes. During the survey of macroinvertebrate grazer, 8 (LB) and 9 (TC) species were observed. Of these, there were 1 gastropod, 2 sea urchin and 5 or 6 sea star species. The abundance of the latter was significantly higher at LB (8.0±2.3 ind. m-2) compared to TC (1.1±0.2 ind. m-2). The pencil sea urchin Eucidaris galapagensis accounted for 99.1 % at LB and 93.4 % at TC of all surveyed macroinvertebrate grazers (Table 2).

77

hpe Grazingeffectss 3 Chapter

Table 1. Analyses of similarity (ANOSIM) and similarity percentages (SIMPER) testing the effects of open vs. closed treatments at each site and between.

ANOSIM (overall) Global R=0.803, p=0.001 LBopen vs. LBclosed TCopen vs. TC closed LBopen vs. TCopen LBclosed vs. TCclosed

ANOSIM R=0.428, p=0.002 R=0.907, p=0.001 R=0.908, p=0.001 R=0.932, p=0.002

SIMPER Dissimilarity 35.7% Dissimilarity 54.1% Dissimilarity 43.6% Dissimilarity 53.4% 8.3%aUnidentfied Anemone 12.1% -Unidentfied Anemone 10.0% +Unidentfied Anemone 9.2% +Ulva 6.1% -Green filam. 9.0% +Ulva 6.5% -Hildenbrandia 5.7% -Hildenbrandia 5.1% -Diatomea 5.8% -Green filam. 6.1% -Lithothamnium 5.5% -Lithothamnium 4.9% +Brown filam. 3.8% a Lobophora 5.5% +Green filam. 4.4% -Brown filam. 4.4% -Red filam. 5.2% a Brown filam. 4.1% p Cyanobacteria 4.4% +Ulva 3.3% +Red filam.

78 Global analysis results of ANOSIM (R, p) testing for both individual and paired treatment differences are also given. Results of SIMPER analysis are given as percent dissimilarity for each significantly different treatment pair, followed by the percent contribution of each single species/taxon to the difference. The table shows all species/taxa that contributed to >30 % of species composition between treatments.

Increased or decreased abundance and absence or presence of each species/taxon with respect to site and treatment (sitetreatment→sitetreatment) are symbolized with +/- and a/p, respectively.

Chapter 3 Grazing effects

Table 2. Results of fish and macroinvertebrate grazer surveys with list of counted herbivorous fishes and macroinvertebrate grazers and their proportion of the respective total count; statistical test and p-values are shown for differences in abundances between both sites (LB and TC).

LB TC

(upwelling) (non-upwelling) Total fish species 43 39 Total individuals 17891 4312 Herbivorous fish species 9 8 ANOVA: Herbivorous fish abundance 0.8±0.1 0.3±0.1 F =12.1, (Ind. m-2 ± SE) 1,14 P=0.004 Species Percentage of total herbivorous fish Nicholsina denticulata 0.2 0.2 Ophioblennius steindachneri 0.5 1.7 Prionurus laticlavius 74.6 60.3 Scarus ghobban 0.4 2.1 Canthigaster punctatissima - 0.2 Girella freminvillei 5.9 0.4 Holacanthus passer 9.5 8.9 Hypsoblennius brevipinnis <0.1 - Microspathodon dorsalis <0.1 - Stegastes beebei 8.8 26.3

Total macroinvertebrate grazer species 8 9 Total individuals 6529 965 Kruskal-Wallis Macroinvertebrate grazer abundance 8.0±2.3 1.2±0.2 test: H =11.3, (Ind. m-2±SE) 1 P<0.001 E. galapagensis abund. (Ind. m-2 ±SE) 8.0±2.3 1.1±0.2 Species Percentage of total macroinvertebrate grazer Coronaster marchenus - 0.1 Linckia columbiae <0.1 - Mithrodia bradleyi - 0.3 Nidorellia armata 0.3 1.4 Pentaceraster cumingi <0.1 0.3 Pharia pyramidata <0.1 0.8 Phataria unifascialis 0.2 0.9 Centrostephanus coronatus 0.4 1.8 Eucidaris galapagensis 99.1 93.4 Hexaplex princeps <0.1 1.0

Discussion

We found different assemblages developing in for each treatment at each site confirming that both grazer pressure and contrasting oceanographic regimes (upwelling vs. non-upwelling) influence rocky reef community structure. The effect of grazer exclusion on species composition was minor at the upwelling site LB compared to the non-upwelling site TC. Following week 12, herbivory favored a strong growth (24 %) of the microalgae D. diatomea at LB, but this species disappeared completely at later

79 Chapter 3 Grazing effects successional stages and was not observed in any plots at TC. However, at the upwelling site LB crustose and filamentous algae dominated coverage with up to 82 % on open plots and 76 % on closed plots. In contrast, grazing at TC diminished obviously the number of major functional groups. Under conditions of grazer exclusion at TC also cyanobacteria, micro-omnivores and corticated terete algae occurred in higher abundances at the late successional stages (after 38 weeks). The presence of cyanobacteria mats under caged conditions was also observed in shallow reefs in the Caribbean (Wanders 1977). Micro-omnivore taxa, such as bryozoans, and certain algae species, such as Caulerpa spp. seem also to benefit from reduced grazing pressure. Hence, cages in this naturally coral-dominated habitat of TC (Krutwa et al. unpublished) excluded not only herbivorous fish, but also non-herbivorous fish species, which feed on epibenthic invertebrates. In general, reef fishes are characterized by a high degree of specialization and were suggested to have the greatest influence on reef structure and dynamics in coral reefs (Hay 1981a,b, Sammarco 1983).

Surprisingly, an unidentified anemone species greatly contributed to the general differences in community composition among treatments, but also between open plots of both sites. The growth of the anemone might be facilitated by grazing, supposedly by outcompeting other algae for space, such as Ulva spp., which might be consumed quickly. Its contribution to community composition was greater on ungrazed plots at the two study sites and the increment of macroalgae and Ulva spp. under grazing reduction is widely known (e.g. Hughes et al. 1987, Smith et al. 2001, Jessen and Wild 2013). Site-specific differences were due to the dominance of crustose algae at the upwelling site LB, and this was previously reported for the same site (Krutwa et al. unpublished). In general, the upwelling site is similar to barren grounds found in temperate regions (Siddon and Witman 2003). Interestingly, foliose algae and Ulva spp., respectively characterized community composition at the non-upwelling site, but played a minor role at the upwelling site even under reduced grazing pressure assuming that upwelled waters, which are characteristically rich in nutrients (Wilkerson and Dugdale 2008), might still be limited by single nutrients (nitrogen or phosphorus) which are necessary for macroalgal growth (Teichberg et al. 2010). Another explanation would be the presence of mesograzers [herbivorous invertebrates smaller than 2.5 cm (Brawley 1992)] on open as well as closed plots. This might have strong impacts on species composition (Duffy and Hay 2000, Nydam and Stachowicz 2007) since such

80 Chapter 3 Grazing effects mesograzers have been observed to live in and to feed on algal turf (Hay et al. 1987, Taylor and Steinberg 2005).

Abundance of herbivorous fish and macroinvertebrate grazers were significantly higher at the upwelling site LB. Sea urchins are key grazers in temperate and tropical regions (Witman and Dayton 2001) and the pencil sea urchin E. galapagensis is the most abundant macroinvertebrate at both sites and the most common sea urchin species in the Galápagos Archipelago (Danulat and Edgar 2002). We found almost 8 times higher abundances of this species at LB and it may be the most structuring species of the benthic communities (Ruitton et al. 2000). These findings also agree with former observations of high sea urchin densities at productive sites in Galápagos (Brandt and Guarderas 2002). Further, experimental studies in the central part of Galápagos showed that E. galapagensis is able to transform algal communities to barren grounds (Irving and Witman 2009, Brandt et al. unpublished). Thus, the occurrence of high abundances of this species might explain the characteristically barren-like structure of the upwelling site in our study. Possibly, the more complex reef structure at this upwelling site also provides more refuge from predation than at the non-upwelling site (Dee et al. 2012), which would be a further reason for the high density of this sea urchin species here.

The proportion of the total count of herbivorous fish differed between sites. While the schooling surgeonfish P. laticlavius (Acanthuridae) accounted for the highest abundance at both sites (60 and 75 % for TC and LB, respectively), the damselfish S. beebei (Pomacentridae) was almost 3 times more abundant at the non-upwelling site TC. These differences in herbivorous fish species proportions could cause different effects on the algal community at both sites. In Galápagos, damselfishes cause discrete patches of filamentous algal turfs and protect them from invading sea urchins (Irving and Witman 2009). Another study on herbivory of the Dusky Damselfish in Southeast Brazil revealed an important trophic role of this species in the system (Ferreira et al. 1998). During our study, small damselfishes frequently entered cages, but were also observed to use the open plates as their territory. Thus, entering damselfishes as well as others cage intruders (such as mesograzers) might have grazed substantially also within grazer exclusion treatments. Similar observations regarding fish grazing were described for a Hawaiian coral reef, where the system passes through either one of two major grazing regimes: that of territorial damselfishes or of schooling parrotfishes and

81 Chapter 3 Grazing effects surgeonfishes (Hixon and Brostoff 1996). The density of herbivorous fishes found at the non-upwelling site LB (8 ind. m-2) was equal to densities found on a coral reef flat in the Red Sea, which showed strong fish grazing effects (Jessen and Wild 2013). In this study, such strong top-down effects were not obvious for the community structure at LB, but very much so for the non-upwelling site TC despite lower grazer densities. Moreover, species-specific effects of grazer and consumer richness effects play an important role in structuring reef communities. For example, a species-rich herbivorous fauna can be crucial for the recovery of coral reefs after disturbances (Burkepile and Hay 2010), or the identity of species may account for most changes in the community structure (Brandt et al. 2012). In addition, it is not clear, how legally extractive activities (artisanal fishing) at LB, influences grazer abundances. For example, Ruttenberg (2001) reported for heavily fished sites lower herbivorous fish abundances and higher abundances of sea urchins.

Species richness was higher at the non-upwelling site TC and on ungrazed plots. At LB, grazer reduction benefited single species, such as Spatoglossum spp. or Nitophyllum spp., which might have been consumed otherwise by the excluded herbivores. Our findings are not consistent with the multivariate model by Worm et al. (2002), where consumers or herbivores increase diversity in high productive systems and decreases diversity at low productive sites. Further, there were no differences in evenness between treatments. Hillebrandt et al. (2007) concluded in a cross-system analysis that herbivory pressure increased producer richness in higher productive sites and in producer communities with low evenness. As a detailed taxonomic analysis of algal groups is lacking in our study, the relationship of these aspects remains unclear. At a broader scale, a case study of subtidal rocky reefs of Australia found that patterns of regional diversity is related to regional variability in productivity and grazing (Connell and Irving 2008).

Conclusions

Our results suggest different ecological mechanisms with a more bottom-up driven system at the upwelling site LB and a more top-down driven system at the non- upwelling site TC within the same biogeographic region. This seems underscored by findings by Witman et al. (2010) for upwelling sites in Galápagos. Strong herbivory

82 Chapter 3 Grazing effects effects at sites of low productivity contrasting to only little effects on communities at high productive sites were also described by Burkepile and Hay (2006) at higher latitudes. Therefore, we suggest that benthic assemblages at LB might be less vulnerable to fishing of herbivorous fish than TC. However, if upwelling is suppressed in these areas during El Niño events the effects on the communities may be severe (Podestà and Glynn 1997, Bruno et al. 2001, Glynn 2001). Further, the interaction of herbivory and seasonality should be considered in future studies. Also herbivory effects may vary with the age of the community and grazing effects on particular successional stages shall be investigated in more detail. As a re-zoning of the GMR is presently considered, an increased knowledge on ecological processes in the GMR appears fundamental for decision makers.

Acknowledgements

The authors thank the Charles Darwin Foundation and the Galápagos National Park Service. AK acknowledges the German Academic Exchange Service (DAAD) for scholarship. Many thanks go to R. Pepolas, J. Delgado, J. Moreno, J. Yépez, S. Clarke and other volunteers for vital support in the field.

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Appendix

Table A1. Species list

Open plots Closed plots No. Taxa/species LB TC LB TC 1 Aplidium solidum x x x x 2 Aplidium spp. x x x x 3 Ascidia spp. x x x x 4 Asparagopsis spp. x 5 Botryocladia spp. x x 6 Bryopsis spp. x x x x 7 Bugula cf. californica x x x x 8 Bugula neritina x x 9 Caulerpa spp. x 10 Caulibugula spp. x 11 Ciocalypta spp. x 12 Cleidochasma porcellanum x x x x 13 Codium spp. x x x 14 Corallina spp. x x 15 Diatomea diatomea x x x x 16 Dictyota spp. x x 17 Didemnum perlucidum x x 18 Didemnum spp. x x x x 19 Eudistoma spp. x x x x 20 Gymnogongrus spp. x x x x 21 Haliclona spp. x x x 22 Schizymenia ecuadoreana x x 23 Hildenbrandia spp. x x x x 24 Hipponix spp. x x 25 Hippoporina verrilli x x x x 26 Hypnea spp. x x x x 27 Isognomon recognitus x x x x 28 Jania spp. x x x 29 Lichenopora intricata x x 30 Lithothamnium spp. x x x x 31 Macrorhynchia philippina x 32 Megalomma mushaensis x x x 33 Membranipora arborescens x 34 Nitophyllum spp. x x 35 Obelia dichotoma x x x 36 Padina spp. x x x 37 Pennaria disticha x x 38 Petalonia spp. x x 39 Peyssonnelia spp. x 40 Pocockiella spp. x x x 41 Psammocora spp. x 42 Pterosiphonia spp. x x 43 Pyura cf. haustor x x x 44 Ralfsia spp. x

89 Chapter 3 Grazing effects

Table A1. continuation…

Open plots Closed plots No. Taxa/species LB TC LB TC 45 Rhynchozoon rostratum x x x x 46 Salmacina tribranchiata x x x x 47 Sargassum spp. x 48 Spatoglossum spp. x x 49 Serpulorbis margaritaceus x x x 50 Thalamoporella californica x 51 Tubastraea coccinea x 52 Ulva spp. x x x x 53 Filamentous brown algae x x x 54 Filamentous green algae x x x x 55 Filamentous red algae x x x x 56 Orange sponge x x x x 57 White sponge x x 58 Polychaete tubeworm x x x x 59 Cyanobacteria x x x 60 Unidentified anemone 61 Unidentified ascidia x x x 62 Unidentified brown algae x x x x 63 Unidentified bryozoan x x x x 64 Unidentified hydroid x x x x 65 Unidentified red algae x x x x

90 Chapter 4 Food web structure

4 First insights into the food web structure of a tropical subtidal rocky reef community (Galápagos, Ecuador) using the stable isotope approach

Carolin M. Herbon, Annika Krutwa

Leibniz Center for Tropical Marine Ecology (ZMT) GmbH, Bremen, Germany ______

Abstract

Over the past decades, the marine ecosystem of the Galápagos Islands has been exposed to the impact of extensive fishing and the extreme climate pattern of El Niño. An irreversible long-term effect on the trophic structure of the system due to these events was predicted by atrophic in silico model on the study area. However, these types of models are constructed of grouped biomass data and a detailed verification on the level of individual units has been lacking. In this study, we used an isotope approach giving a more defined and accurate output of the food web focusing on single species. With this technique, we evaluated the food web structure of subtidal rocky reef communities off the island of Floreana. Six abundant species and four possible food sources of the system were collected and analyzed for carbon and nitrogen content as well as their stable isotopes. Results revealed three trophic levels and thereby confirmed and complemented the findings of the trophic model. For a solid evaluation of the food web structure, a combination of both methods is recommended in particular when exploring the impact of commercial uses and management strategies of key species. To our knowledge, this is the first study to analyze food webs using an isotopic approach in the Galápagos marine system and the first isotope study on the tube feet of Asteroidea.

Keywords: benthic food webs; Floreana; Galápagos; stable isotope ecology ______

91 Chapter 4 Food web structure

Introduction

The Galápagos Archipelago is located in the Eastern Tropical Pacific, about 1000 km west of Ecuador’s mainland coastline and lies in a complex transition zone between tropical, subtropical, and upwelling waters (Schaeffer et al. 2008). This particular and isolated setting of the archipelago provoked the development of unique, diverse and complex but poorly understood marine and coastal ecosystems (Houvennagel 1984, James 1991). Between three and five major biogeographic regions were identified for the Galápagos Archipelago (Harris 1969, Jennings et al. 1994, Wellington et al. 2001, Edgar et al. 2004). The central-south zone is the largest biogeographic region of the Archipelago with a remarkable regional mix of marine species demonstrating temperate and subtropical bioregions (Edgar et al. 2004). Floreana Island, located in the central- south, is the sixth largest island and its shallow rocky reefs are typical of the central- south Galápagos reef ecosystem (Bustamante et al. 2008). The shallow-water rocky reef ecosystem around Floreana is characterized mainly by sloping lava fields with sandy pocket beaches (Okey et al. 2004) and an exceptionally diverse combination of warm- and cool-water species (Witman and Smith 2003).

In recent decades, major ecological changes were observed for the Galápagos Islands (Glynn 1994) caused by increased fishing pressure and strong El Niño events (Edgar et al. 2009). These anthropogenic as well as natural impacts can influence the trophic structure of a system (Lindberg et al. 1998) and can in fact lead to shifts within the ecosystem (Scheffer et al. 2001). For Galápagos, a conceptual model postulates the following three-level trophic cascade. Firstly, a decrease in abundances of lobster and large predatory fish and others through fishing pressure; secondly, an increase in densities of macroinvertebrates and in particular the pencil sea urchin Eucidaris galapagensis following reduction of predators; and thirdly, a decline in macroalgae and coral cover when stresses are accompanied with strong El Niño events combined with high densities of grazing invertebrates (Edgar et al. 2009, Sonnenholzner et al. 2009). Hence, macroinvertebrates seem to play a key role in Galápagos benthic food web structure: on the one hand, lobsters and sea cucumbers (as such Isostichopus fuscus) as a lucrative fishery resource (Hearn et al. 2005, Hearn et al. 2007) and on the other hand, the most common sea urchin species E. galapagensis (Danulat and Edgar 2002), which

92 Chapter 4 Food web structure is an omnivore known also to graze on corals (Glynn 1979, Reaka-Kuda et al. 1996), as a habitat forming species.

In order to predict changes in the food web structure due to changing predator/prey relationships, trophic interactions of key species should be examined. Further, it is important to understand the complexity of interactions in this system. The distribution of species over trophic levels within a benthic community provides important information about hierarchies and the transfer of carbon and nitrogen. The length of the food chain is determined by several factors, such as ecosystem size and species richness, and can help to quantify trophic structure (e.g. Michener and Schell 1994; Vander Zanden and Rasmussen 1999, Lepoint et al. 2000, Abrantes and Sheaves 2009). In intertidal communities, usually three to four trophic levels are distinguished (e.g. Bouillon et al. 2002, Abrantes and Sheaves 2009). During the last three decades the analysis of stable isotopes proved to be a very useful tool in investigating benthic communities (Peterson and Fry 1987, Dauby 1990, Riera et al. 1999, Yoshii 1999; Lepoint et al. 2000). Within the scope of the stable isotope approach, carbon and nitrogen are the most appropriate elements to compare species positions in an ecosystem (Post 2002). This method is based on the fact that the heavy isotopic fraction is increasingly accumulated with each trophic level (Gannes et al. 1998). The carbon isotopic composition contains the information about the carbon source within a food chain, whereas the nitrogen isotopic composition is a sufficient tracer for trophic levels (Caut et al. 2009). Isotopically light 14N is decomposed and excreted more easily as faeces or in form of urate (Gannes et al. 1998).Therefore,15N is enriched in the animal’s body. Furthermore, background information of previous studies, e.g. investigating food preferences, is additionally used to build a picture of the food web structure.

The food web structure of the shallow-water rocky reef system of Floreana was characterized by Okey et al. (2004) and Bustamante et al. (2008) by constructing a balanced trophic model using Ecopath with Ecosim (Christensen et al. 2000). According to these, the system of Floreana has been strongly altered by fishing. Furthermore, the overall food web is described as more heterotrophic in spite of its high benthic production rates and biomass.

Here, we analyzed stable isotope signatures of seven characteristic species and two food sources of shallow rocky reef habitat off Floreana Island in order to obtain

93 Chapter 4 Food web structure information on the trophic structure of the benthic food web. In detail, we expect little or no terrestrial input of primary carbon sources. Results of this study were compared with findings given by the mass-balance model approach by Okey et al. (2004). To our knowledge, this is the first study on food web structure based on the stable isotope approach for the Galápagos rocky reef ecosystem.

Material and Methods

Sample collection and preparation Samples were taken in March 2011 in the frame of a two year monitoring project at two sites off Floreana Island, namely La Botella (90º 29' 55.92'' W, 1º 17' 25.16'' S) and Tres Cuevitas (90º 24' 30.26'' W, 1º 14' 6.45'' S). Ten species and food sources were chosen as study objects. Two fish species (Stegastes beebei, Prionurus laticlavius), four invertebrates (Gastropoda: Conus nux; Echinoidea: E. galapagensis, Holothuroidea: I. fuscus, Asteroidea: Nidorellia armata) and four different food sources [sediment surface, filamentous algae, Ascidia sp., Aplidium solidum) were collected. If available, three organisms of each species were collected at each site (Table 1).

Table 1. Number of sampled replicates (n) for each species.

Species n Conus nux 5 filamentous algae 2 Eucidaris galapagensis 2 Stegastes beebei 2 Prionurus laticlavius 2 Isostichopus fuscus 4 Nidorellia armata 2 Ascidia sp. 4 Aplidium solidum 4 sediment surface 6

Muscle tissue was taken from the fishes and the invertebrates if possible. Soft tissue of the Gastropoda was sampled as a whole due to their low dry weight. From the Holothuroidea the muscle tissue of the anus was sampled. In case of the Asteroidea the tube feet were sampled, as their body did not provide enough soft tissue for analysis. The food sources were taken as a whole and rinsed with distilled water before further treatment. All samples were then dried in the oven at 40° C and homogenized with an

94 Chapter 4 Food web structure agate mortar. Sediment samples were dried at 40° C, treated with 200μl 1M HCl to remove carbonates and then redried. Subsamples were analyzed for organic carbon 13 (Corg) and nitrogen (N) and also stable isotope composition of organic carbon (δ Corg) and nitrogen (δ15N).

Stable isotope analysis

Samples were combusted in a Carlo Erba NA 2100 Elemental analyzer for Corg and

Ntot measurements. Stable isotope ratios were determined using a coupled EA-IRMS gas isotope ratio mass spectrometer (ConFlo III) and expressed relative to conventional standards:

X samples _ δR= ( 1)* 1000 l (1) Xstandard

with R= 13C or 15N and X= 13C/12C or 15N/14N. Ammonium sulfate (IAEA-N1, IAEA-N2) was used as standard for δ15N, and graphite (USGS-24) and mineral oil (NBS-22) for δ13C. Analytical precision was ±0.2 ‰ for both nitrogen and carbon, as estimated from standards analyzed together with the samples.

Results

The percentual carbon and nitrogen values are mirrored in the food web structure considering the isotopic composition of the organisms (Figure 1). Exceptions are the sediment samples as well as the filamentous algae, which have comparably high 15N:14N ratios. They also show higher C:N ratios (C:Nsediment=19,18; C:Nfil.algae=202,41) than the other sampled groups, where C:N ratios were below 12. δ13C of primary food sources are ranging between -19.91 ‰ to -6.82 ‰.

Previous studies examined that carbon isotopic composition differs between predator and prey by 0.8‰ (e.g. Sheaves and Molony 2000, Vander Zanden and Rasmussen 2001). Nitrogen on the other hand proved to be a sufficient tracer for trophic levels, as heavy nitrogen (15N) is accumulated with each trophic level and the isotopically light 14N is easier decomposed and excreted as faeces or in form of urate. Caut et al. (2009) showed that the enrichment to the next trophic level is about 2.8 ‰. In an experimental approach by Herbon and Nordhaus (2013) however, it was also said

95 Chapter 4 Food web structure that these values cannot be generalized for all organisms, as they found higher discrepancies between trophic levels. It is therefore important to take background knowledge of study organisms and their feeding behaviour as well as findings from previous ecological studies into account. Based on our findings, we can assume three trophic levels apart from the primary carbon sources (Table 2).

Figure 1. Percentual (a) and stable isotope values (b) of carbon and nitrogen of sampled species [Fish: S. beebei (SLE), P. laticlavius (PLA); Gastropoda: C. nux (CNU); Echinoidea: E. galapagensis (EGA); Holothuroidea: I. fuscus (IFU), Asteroidea: N. armata (NAR); Food sources: sediment surface (SED), filamentous algae (FAL), Ascidia sp. (ASC), A. solidum (ASO)].

Table 2. Comparison between estimated trophic levels by using the stable isotope approach (TLI) and the Ecosim with Ecopath approach (TLE) by Okey et al. (2004).

Species TLI TLE Conus nux 2.0 3.0 Stegastes beebei 3.0 2.7 Prionurus laticlavius 3.0 2.4 Eucidaris galapagensis 2.0 2.2 Isostichopus fuscus 1.0 2.1 Nidorellia armata 2.0 2.5 Ascidia sp. 0 (1)a 2.0 filamentous algae 0 (1)a 1.0 Aplidium solidum 0 (1)a - Sediment 0 (1)a - a Stable isotope approach defines primary carbon sources as TL=0, whereas the Ecosim with Ecopath approach sets primary producers TL=1

Discussion

All C:N ratios calculated in this study are below 12, except for those of the filamentous algae and the sediment. Bouillon (2002) suggested that C:N values higher than 12 indicate a large contribution of terrestrial carbon, whereas lower C:N ratios

96 Chapter 4 Food web structure combined with high δ13C values indicate an import of carbon to the system. Due to the fact that river run-off is completely lacking in Floreana and mangrove habitats are also limited, we anticipated little or no terrestrial input of primary carbon sources. This was confirmed by the C:N ratio obtained in this study and means that the food web in our sampling sites relies totally on imported carbon from the water column, such as e.g. from microalgae. This is also confirmed by the respective high δ13C values. Filamentous algae have the highest measured δ13C values in this study. They are most probably the explanation for the generally high δ13C values in this system, as it can be assumed that they contribute largely to the diet of the first trophic level. Another well-known food source for the benthic community of this area is the macroalgae Ulva spp., which could not be sampled during our expedition, as only a thin layer was found growing on rocks at that time of the year (warm season). During the cold season, this species can be found in higher biomasses (Krutwa, personal observation) and therefore also contributes as a primary carbon source to the benthic food web. It is generally known, that macroalgae cover changes in response to seasonal cycles (Diaz-Pulido and Garzón-Ferreira 2002, Prathep et al. 2007) and hence, may affect the food web structure. Consequently, sampling time and seasonality have to be considered when analyzing the food web structure.

For the examined organisms, we distinguished three trophic levels. The first trophic level is represented by I. fuscus, a Holothuroidea. δ15N values for Holothuridea vary strongly in different studies (4.1 to 11.8 ‰), depending on the habitat and species food preferences (Davenport and Bax 2001, Yokoyama et al. 2005, Behringer and Butler 2006, Grall et al. 2006, Jacob et al. 2006, Nadon and Himmelmann 2006, LeLoch et al. 2008). The δ15N values in our study were in an average range with 5.71±0.37 ‰. Holothuroidea mainly feed on sediment, detritus and microalgae (Davenport and Bax 2001). As the δ15N values for sediment were slightly higher (6.95±0.62 ‰) in our study compared to others (e.g. France 1998, Bouillon et al. 2008), an enrichment of the sediment with 15N is indicated. The sources of this 15N in our study sites are microalgae that cover the sediment completely in some parts of this area (personal observation). Secondly, it can be assumed that the sediments contain remains of dead animal material, which is highly enriched in 15N (Thongtham and Kristensen 2005, Kristensen et al. 2010). Feeding on such sediment explains the high values we measured for the sea cucumber I. fuscus. Holothuroidea are the food source of e.g. the spiny lobster (Marx

97 Chapter 4 Food web structure and Herrnkind 1985; Behringer and Butler 2006) or pinnipeds (Hobson and Welch 1992), which occurs in high abundances around the Galápagos Islands (Holthuis and Loesch 1967, Trillmich 1979, Bustamante et al. 2000).

The gastropod C. nux, the sea star N. armata and the sea urchin E. galapagensis were found to form the second trophic level. Their δ15N values were measured to be between 8.77 and 8.92 ‰. The main food sources of these three species are sediment, microalgae and probably additional 15N enriched sources, such as animal tissue that they take up by occasional scavenging. They are highly abundant in this benthic community. Hobson et al. (2002) found similar δ15N values for other species of Echinoidea (8.3±0.5 ‰) but much higher values for Asteroidea (12.7±0.4 ‰). δ15N values for gastropods are varying strongly (Hobson et al. 2002, Takai et al. 2004), as the isotopic composition in this group depends highly on the species and its diet, as they can be both herbivorous and carnivorous. C. nux, in the Galápagos Islands, is an omnivorous species that preferably feeds on polychaetes and other worms (Nybakken 1978), which explains their occurrence on the second trophic level within this food web.

Studies containing data of isotopic values for Asteroidea are rare. Furthermore, to our knowledge, studies on isotopic compositions for tube feet in comparable habitats are completely lacking. In a fatty acid composition study with deep sea Asteroidea, samples were also taken from the tube feet (Howell et al. 2003). They found Asteroidea to be mud or suspension feeders with a high contribution of bacteria to the carbon source. Weber (1968) analyzed several species for carbon isotopic composition, but used only skeletal elements for analysis. He found much higher values for δ13C than in our study, varying from -8.19 ‰ to -5.07 ‰, depending on the species and the skeletal element sampled. It was concluded that these high δ13C values are not related to the diet, but rather to an isotope exchange between the metabolic carbon dioxide and dissolved bicarbonate near the site of deposition of carbon in the skeleton (Weber 1968). δ15N values for Asteroidea in a study by Jacob et al. (2006) range between 6.07 and 11.39 ‰, but without information on the body part sampled. As their δ13C differ largely from values in our study, comparison is therefore difficult. Previous studies have shown that Asteroidea feed on bulk sediment that includes meiofauna, fecal pellets, bacteria and nutrients from organic detritus, and furthermore, that they scavenge on larger animals (Madsen 1961, Shick et al. 1981, Jangoux 1982, Billet 1987). The clear distinction that

98 Chapter 4 Food web structure primary consumers are herbivorous only, secondary consumers are carnivorous etc., such as stated by Minagawa and Wada (1984), therefore does not necessarily apply.

A previous study on sea urchins showed that they can appear on different trophic levels (Vanderklift et al. 2006). Thus, the trophic level depends highly on the given food sources in the area of interest, as well as on the individual food preferences of the species. On the one hand, the δ15N values of E. galapagensis in our study were higher than values for other species of Echinoidea in salt-marsh or mangrove-seagrass-coral habitat studies (Lesage et al. 2001, Moriniere et al. 2003). On the other hand, similar δ15N values for Echinoidea were found by Tomas et al. (2006) in seagrass beds, where - according to the stable isotopes measured- the sea urchin Paracentrotus lividus preferentially consumed epiphytes. In Galápagos, the dominant pencil sea urchin E. galapagensis is known to be a corallivore, having a great impact on algal-covered carbonate surfaces (Glynn 1994, Reaka-Kuda et al. 1996) and also to be highly adapted to changes in oceanographic conditions (Glynn 1994). It may therefore be able to easily adapt to changes in type and quantity of natural food sources. The main consumer of E. galapagensis is the spiny lobster (Sonnenholzner et al. 2009).

The third, and in our study highest, trophic level is formed by the two fish species S. beebei and P. laticlavius, which are both omnivorous. A former study by Ho et al. (2007) measured similar isotopic values for carbon and nitrogen in Stegastes fasciolatus (Ogilby 1889). They found macroalgae, epiphytic algae and detritus to be contributing the largest part of the analyzed food items to the stomach content, whereas about 30 % were covered by diatoms, amphipods, polychaetes and fish eggs. Due to the fact that the degree of isotopic fractionation is not to be generalized for all organisms, as suggested by Herbon and Nordhaus (2013), we can assume that S. beebei in fact mainly feeds on macro- and epiphytic algae (Ruttenberg et al. 2005), although it shows such high values for δ15N. As mentioned before, macroalgae cover at sampling sites increases during the cold season. In the hot season, the epiphytic algae as well as the sediment including detritus, polychaetes and other algae are probably the main food sources for these fish species.

As summarized in a study by Iken et al. (2001), the analyzed groups can be divided into predators or scavengers (including Pisces, Gastropoda and Asteroidea), deposit feeders (including Holothuroidea, Echinoidea and also Asteroidea) and suspension

99 Chapter 4 Food web structure feeders (Tunicata). This allocation is based on the nitrogen isotopic composition, as well as background knowledge about feeding habits, as isotopic composition alone cannot give a clear structure of the food web because the interactions between trophic levels are too complex.

Okey et al. (2004) and Ruiz and Wolff (2011) investigated the Galápagos food web with a trophic model approach. They created a simplified balanced model of this system, based on biomass density estimations from previous studies and their own survey data. Further input parameters, production/biomass and consumption/biomass ratios as well as diet composition, derived mainly from the scientific literature and FishBase (Froese and Pauly 2011). Then, representative data for every functional group were used to feed the model. As can be seen from table 2, findings of the modeling approach fit largely to the outcome of the isotope measurements that were evaluated with additional background knowledge of feeding habits. However, some of the species were defined to occur on other trophic levels than in our study, or differed slightly. This could be explained by the small amount of replicates in our study, but can also be a result of different feeding habits during this time of the year, as food availability and quality alternates over the year, depending on the season. As was already discussed above, high variance can also occur within the same species. The species in the trophic model are grouped in a way that individual species are not examined. Therefore, it depends highly on the level of interest, which method (trophic modeling or isotope analysis) is appropriate to answer the study question.

In general, a comparison between discrimination factors of different studies or isotopic compositions of similar species remains difficult as values between body tissues within one individual can already differ significantly (Waddington and McArthur 2008). In most cases, tissues investigated remain unspecified. This can result in different food web structures and discrimination factors between predator and prey. A generalization of the value of isotopic fractionation between two trophic levels, as suggested by Vander Zanden and Rasmussen (1999), is therefore not possible and in many cases the occurrence in a certain trophic level does not necessarily allow a conclusion on the feeding habit of a species (Herbon and Nordhaus 2013). The complexity of food webs does not allow the partitioning of species into herbivores or carnivores, as in most cases an omnivorous feeding behavior is on hand, whereas the

100 Chapter 4 Food web structure herbivorous or carnivorous contribution can differ. Eventually, this depends highly on the habitat, food availability and the species (Hobson et al. 2002, Jacob et al. 2006, Vanderklift et al. 2006, Waddington et al. 2008).

Conclusions

Although or even because the balanced trophic model is simplified, it allows an integrated description of the food web structure of a given system. However, the stable isotope approach examines the actual trophic levels of the target species and food sources, which may be particularly relevant in a highly dynamic system like Galápagos. Thus, a combination of trophic modeling and experimental studies on stable isotopes would be appropriate for a more reliable and realistic picture of the benthic food web structure. This is also essential for appropriate management planning.

In the future, a more detailed isotopic investigation on Floreana Island should be conducted with a higher resolution of sampling sites and a higher number of species and replicates. In order to catch the seasonal dynamics of the system, further investigations during the cold season should be conducted.

Acknowledgements

The authors acknowledge the financial support from the International Office of the German Federal Ministry of Education and Research (BMBF, Grant No. ECU 10/A01). Thanks go to the Charles Darwin Foundation for administrational support and to the Galápagos National Park Service for permits. We thank Jennifer Suarez and Diego Ruiz for vital help during field work and to Dorothee Dasbach for laboratory work and support. Helpful comments of referees are thankfully acknowledged.

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108 Synthesis

Synthesis

Subtidal rocky reef communities of Floreana Island Small-scale variations in community structure, Shannon diversity (Chapter 1), succession patterns (Chapter 2) and grazing effects (Chapter 3) were found in the investigated subtidal rocky reef communities of Floreana Island. The observed differences of the benthic communities at the study sites La Botella and Tres Cuevitas were related to their contrasting oceanographic regimes, which consisted of strong upwelling events on the one hand and the absence of upwelling on the other hand. Temporal variations, i.e. between the cold and the warm season, were evident only for the sessile community structure at the non-upwelling site, whereas at the upwelling site seasonality had no effect at all (Chapter 1).

The subtidal rocky reef community at La Botella is characterized by crustose algae like Lithothamnium spp. and Hildenbrandia spp. (Chapter 1, 2) and high abundances of the pencil sea urchin E. galapagensis (this study, 8.0±0.1 ind. m-2) and herbivorous fish (this study, 0.8±0.1 ind. m-2) (Chapter 3). Due to strong upwelling events at this site (Witman et al. 2010) a more macroalgae-dominated reef could have been expected. Banks et al. (2012) mentioned that there might be a threshold level of densities of E. galapagensis, at which a regeneration of macroalgal assemblages is limited, and assumed an average of 3.2 individuals per m2 to be an indicator of the development of urchin barrens in the central part of the Archipelago. However, the exclusion of grazers did not lead to the development of a macroalgae habitat at La Botella, suggesting minor top-down effects and a more bottom-up driven system (Chapter 3). In contrast, the non- upwelling site Tres Cuevitas is characterized by reef-building corals such as P. gigantea and P. clavus with significantly higher coverage of filamentous algae and macroalgae than at La Botella (Chapter 1). There, grazing pressure, despite significantly lower grazer abundances than at the upwelling site, had strong impacts on the community structure (Chapter 3). The high variability of ecological processes - which are tightly linked to oceanographic features - within one single biogeographic region was emphasized also by the varying patterns of succession (Chapter 2). The developing assemblages at La Botella soon resembled the surrounding natural community, while at Tres Cuevitas it will take much longer to recover due to slow-growing hard corals and

109 Synthesis low recruitment rates. Since community structure of the natural and developing communities differed at the end of the experiments, it is likely that recovery may take longer than two years. However, it can be deduced that benthic communities might recover at different rates depending on the oceanographic regime.

A total of 154 taxa were found during the study (Table A1), of which filamentous algae were classified in three categories of filamentous brown, green and red algae and not further identified. Therefore, the total number of taxa monitored is rather underestimated since other studies on algal turf, i.e. small filamentous algae, have shown highly diverse assemblages (e.g. Fricke 2011). For the central-south bioregion, about 800 species were reported (Banks et al. 2012), including soft-bottom communities. However, rocky reef communities represent the greatest part since more than 80% of the shallow habitats in the Galápagos Marine Reserve (GMR) are rocky reefs and the total GMR species numbers add up to 3,155 of which 390 taxa belong to the soft bottom habitat (Banks et al. 2012).

Bustamante et al. (2008) described Floreana Island’s system as strongly altered by fishing. Indeed, in the present study few ‘pepino’ sea cucumbers (Isostichopus fuscus) and lobsters were observed. The population of I. fuscus is actually overexploited (Toral- Granda 2008) and the extraction rates of sea cucumbers and lobsters are not sustainable anymore (Okey et al. 2004). During the present study almost no recruitment of lobsters and sea cucumbers occurred at both study sites (Ruiz and Moreno, unpublished data), which confirms the lack of these macroinvertebrate species at Floreana Island. Information about fishing targets and capture rates at the study sites was not available. Tres Cuevitas is located within the conservation subzone, although illegal fishing is still reported for the GMR (Banks et al. 2012), whereas at La Botella extractive activities are allowed. However, during field trips fishing boats were not present although both sites are close to the harbor of Floreana Island. If it is assumed that La Botella is a frequently fished site and Tres Cuevitas is not, high abundances of the sea urchin E. galapagensis can be explained by the lack of their predators (Sonnenholzner et al. 2009). In which way the depletion of certain target species changes the food web structure can be explained by a trophic modeling approach (e.g. Ecopath with Ecosim, Christensen et al. 2000), but also by using stable isotopes. The latter method examines the actual trophic level of target species and food sources. This may be especially relevant for the

110 Synthesis

Galápagos ecosystem, which is highly dynamic and influenced by anthropogenic (e.g. fishing) and natural (e.g. ENSO) impacts. Here, three trophic levels were distinguished by using the stable isotope approach (Chapter 4), but findings differed slightly from those described by a balanced trophic model approach by Okey et al. (2004). Therefore, a combination of both methods would be recommendable, not only to reduce uncertainties in the reconstruction of the model (Lassalle et al. 2014).

Environmental parameters Temperature records of study sites confirmed the known distinction of the two seasons, the cold season from June to November and the warm season from December to April. Furthermore, the mean temperature differed between both sites (Chapter 1), showing that the upwelling site La Botella is shaped by cooler waters than the non- upwelling site Tres Cuevitas. Prior to this project, appropriate study sites were chosen according to the description by Banks (2003) (see Figure 1). Further, upwelling intensity and chlorophyll a values were described by Witman et al. (2010) for La Botella, which was characterized as a strong upwelling site with chlorophyll a concentrations between 1.1 and 1.5 mg m-3. For comparison, a study in the Great Barrier Reef measured chlorophyll a concentrations between 0.4 and 0.8 mg m-3due to upwelling intrusions (Andrews and Gentien 1982). Consequently, La Botella can be regarded as a site of high productivity. Unfortunately, nutrients measurements at study sites had to be discarded due to incorrect analysis. However, the lack of frequent upwelling events that results in less nutrient supply (Witman and Smith 2003) (Chapter 1, Figure 2) indicates that Tres Cuevitas is characterized by warmer waters with less productivity.

111 Synthesis

Figure 1. Interpolated temperatures to depth across 26 sampling stations spaced at 1 km intervals from west-north-eastern Floreana (26/09/2002) modified from Banks (2003).

Floreana – a small-scale picture of the larger biogeographic patterning of the GMR? The GMR is a highly complex and dynamic system, where these spatial and temporal variations of subtidal rocky reef communities do not only occur between larger biogeographic regions but also on small scales of a few kilometers within the same biogeographic region (Danulat and Edgar 2002, Edgar et al. 2004). As mentioned before, Floreana Island is located in the central-south biogeographic region, which is characterized by an exceptional mixing of warm- and cool-water biota (James 1991, Witman and Smith 2003, Edgar et al. 2004). In the present study, a species overlap of about 56.5 % was evident, i.e. more than 40 % occured only at one site or the other (Chapter 1). Examples of exemplary warm-water species, which were exclusively found at the non-upwelling site, are the zooxanthellate corals P. gigantea and P. clavus. In contrast, sponges like the subtropical Cliona chilensis were only found at the cool, upwelling site. Certainly, dense macroalgal beds like in the western part of the Archipelago (Ruiz and Wolff 2011) or coral species assemblages like in the far northern islands (Banks et al. 2009) are missing in the shallow reefs of Floreana Islands. Nevertheless, the Floreana ecosystem represents just as a “model ecosystem” for investigating how the oceanographic regime influences communities on small scales, as

112 Synthesis the entire Archipelago does on meso- and large scales (Witman et al. 2010, Vinueza et al. 2013).

The ecosystems of the GMR with their diverse communities and great proportions of endemism are unique in the world, making global comparisons, as often done for coral reefs, mangrove forests and seagrass habitats, difficult. Hence, the marine communities of the Galápagos Islands require a closer look within the context of their isolated and particular oceanographic setting and may serve as a natural laboratory. For instance, it has been supposed that coral reef structures in the Galápagos due to their location in ocean acidification hot spots represent a “real-world example” of the consequences of climate change (Manzello 2009, 2010).

Horizontal vs. vertical habitat Substrate angle is an important factor for the structure of the benthic community, i.e. “dominance by algae versus invertebrate” (Witman and Dayton 2001). In general, horizontal substrata are dominated by macroalgae, whereas vertical walls tend to be covered by epifaunal invertebrates (Witman and Sebens 1988, Bruno and Witman 1996). At La Botella, a vertical rock wall was present and covered by diverse faunal assemblages consisting of black corals, gorgonians, sponges, barnacles, tunicates and others (Witman et al. 2010, personal observation), whereas crustose algae like Lithothamnium spp. and Hildenbrandia spp. dominated the horizontally orientated assemblages (Chapter 1). This is mainly due to higher light levels on horizontally than on vertically orientated substrate, which favor the survival and growth of macroalgae (Baynes 1999, Witman and Dayton 2001). At the non-upwelling study site Tres Cuevitas no extended vertical structures were existent.

Subtidal vs. intertidal Communities living in the intertidal shore are exposed to extreme conditions. Diurnal cycles of rising and falling tides cause a regular shift between marine and terrestrial habitat. Further, seasonal conditions in combination with low tides can have drastic effects on the organisms (Gili and Petraitis 2009). For example, winter low tides in the Gulf of Maine often expose communities to temperatures below the freezing point or summer low tides in Australia expose them to exceptionally high temperatures (Gili and Petraitis 2009). In addition, wave surge also varies seasonally and affects for example the distribution of organisms by expanding the extension of the intertidal zone

113 Synthesis

(Dayton 1971). In contrast, shallow subtidal habitats are less susceptible to diurnal cycles and wave action, shaping communities made up of organisms which are less adapted to extreme conditions. However, seasonality also affects communities in sublittoral habitats, although this may vary between macroalgal- and faunal- dominated communities (Turón and Becerro 1992, Gili and Petraitis 2009).

In Galápagos, the lava rocky shores constituting about 1800 km of the coastline (Snell et al. 1996) are a prominent feature of the marine environment and their inhabiting communities are greatly sensitive to climatic variations (Vinueza et al. 2006). Although former studies suggested strong grazing pressure for the tropics (e.g. Menge and Lubchenco 1981, Burkepile and Hay 2006), a recent large-scale study in the Galápagos intertidal ecosystem revealed that grazing (top-down) effects were strongest in areas of low productivity and that these effects were mitigated in areas of higher productivity (Vinueza et al. 2013). In the present study, a similar pattern was observed in subtidal habitats with stronger effects of herbivorous fish and sea urchins at the non- upwelling (less productive) site Tres Cuevitas than at the upwelling site La Botella (Chapter 3). Moreover, Vinueza et al. (2013) described temporal variations in top-down effects, which prospectively should be analyzed for Galápagos subtidal habitats (Krutwa et al. unpublished data).

Implications for conservation The shallow rocky reefs of Floreana Island are known to accommodate not only a diverse mixing of cool- and warm water species (James 1991, Witman and Smith 2003), but are also a refuge for threatened species (Edgar et al. 2008). At the study sites, some rare and/or threatened species were found, for example, the coral Gardineroseris planulata, which was registered at Tres Cuevitas in December in 2008 (Figure 2-C). Patches of this coral species survived El Niño of 1982/83 but then disappeared during El Niño of 1997/98 (Hoeksema et al. 2008) and was assumed to be locally extinct. At the same site, the sea star Coronaster marchenus (Figure 2-A) was found during the succession study underneath the experimental lava plates and was recently rediscovered in 2002. Further, at the upwelling site La Botella the red alga Schizymenia ecuadoreana was observed during the cold season in this study (Figure 2-B). This critically endangered alga was reported before at only three sites (Floreana, Isabela and Fernandina Islands) and is endemic to the Galápagos Archipelago (Miller et al. 2007,

114 Synthesis

Edgar et al. 2008). These findings highlight the importance of the subtidal rocky reef habitats off Floreana Islands as a refuge for threatened species and for the conservation of biodiversity in the GMR.

Figure 2. Photos showing A) Coronaster marchenus B) Schizymenia ecuadoreana C) Gardineroseris planulata D) bleached Pocillopora sp. in front with Pavona clavus in the back (Photos B and C kindly provided by DJ Ruiz).

Edgar et al. (2008) suggested the protection of so called Key Biodiversity Areas in the GMR. These sites were identified according to the occurrence and persistence of threatened species, which particularly reflect a great proportion of the global population and thus are of global significance for conservation.

The GMR is subjected amongst other threats to the introduction of invasive species (Banks et al. 2012). In the present study, at least three established potentially invasive species were found: the brown bryozoan Bugula neritina, the Christmas tree hydroid Pennaria disticha and the grape alga Caulerpa spp. (Inti Keith, personal communication). Hence, further investigations have to be carried out to determine the distribution and abundance of potentially invasive species in the Floreana marine

115 Synthesis ecosystem and their possible effect on the benthic communities. Floreana Island is popular for its amazing diving and snorkeling sites and tourists boats often run between the islands. It is unclear, whether and how these activities favor the introduction of invasive species in the GMR.

Since the present findings show that recovery rates depend on the oceanographic setting (Chapter 2), conservation measures might have to include oceanographic processes. On the one hand, because the recovery at the upwelling site La Botella is likely to be faster than at the coral-dominated, non-upwelling site Tres Cuevitas, the latter site needs elevated protection from further disturbances (e.g. fishing and tourism). On the other hand, the upwelling site may promote higher productive output for sessile filter-feeding organisms and therefore the continuity of consumers (Witman and Smith 2003). For upwelling sites, Witman and Smith (2003) suggested the greatest turnover in subtidal sessile invertebrate communities in completely protected areas of the GMR. Furthermore, the authors also emphasized the importance of considering the interaction of oceanography and biotic interactions when management strategies (re-zoning) are developed.

As aforementioned, the marine ecosystem of Floreana Island has been strongly altered by fishing (Bustamante et al. 2008). In combination with ENSO events fishing can greatly raise the extinction risk of marine species in the GMR (Edgar et al. 2009). Therefore, adequate measures have to be applied in order to at least mitigate the negative impacts on communities, although they will not be completely eliminated during ENSO events (Edgar et al. 2009, Figure 2-D).

In the recent past, the Galápagos National Park took actions to better protect the GMR for instance by re-structuring visiting sites and thus to ameliorate the tourism pressure on formerly highly visited locations. This year, in 2014, a new law of the ban of plastic bags in the Archipelago will be initiated by the National Park and the Ecuadorian Government in order to decrease the pollution in the islands.

Accomplishment of research objectives 1) Subtidal rocky reef communities of Floreana Island in the GMR were investigated and differences were evident for the sessile, mobile macroinvertebrate and fish community between the upwelling (La Botella) and

116 Synthesis

non-upwelling site (Tres Cuevitas). Diversity (H’) and evenness (J’) were higher at the non-upwelling site, which was dominated by habitat-forming corals, for all three studied organism groups. Nevertheless, no significant differences were found in species richness (S). Coverage of filamentous algae and macroalgae were higher at the non-upwelling site, whereas coverage of calcareous and encrusting algae was lower than at the upwelling site. Seasonal changes in benthic community structure occurred at the non-upwelling site for the sessile organisms group suggesting well-adapted species to temperature changes at the upwelling site (Chapter 1)

2) The succession patterns differed between the upwelling and the non-upwelling site. At La Botella, a more predictable succession was observed, where the developing community resembled the surrounding natural community after less than two years. In contrast, at Tres Cuevitas the succession was characterized by a more random pattern resulting in a slower recovery rate due to slow-growing hard corals and low recruitment (Chapter 2).

3) The grazer community differed in composition and abundances between sites. Although higher abundances of grazers were found at the upwelling site, grazing effects were less than at the non-upwelling site, where grazer abundances were lower. Thus, a more bottom-up system is suggested for the upwelling site, whereas a more top-down driven system was found at the non-upwelling site. Clear patterns in grazing effects on diversity were not evident for both sites (Chapter 3).

4) The results of the stable isotope approach revealed three trophic levels of the food web in Floreana rocky reef communities. Findings agree widely with trophic modeling outputs by Okey et al. (2004), but a combination of both methods is recommended for further food structure studies (Chapter 4).

5) The subtidal rocky reef ecosystem of Floreana can be used as a “model ecosystem” for investigating how the oceanographic regime influences communities on small scales. Because of their contrasting abiotic environments and the occurrence of a mixing of species belonging to warm- and cold-water bioregions it represents a small-scale example of the entire Archipelago.

117 Synthesis

Furthermore, Floreana Island serves as a refuge for threatened and rare species in the GMR and is of high conservational concern due to fishing pressure, invasive species, tourism and climate variations (Synthesis).

Conclusion and outlook As in the subtidal habitat little knowledge exists on how upwelling affects the communities (Witman and Smith 2003), this thesis represents the first comprehensive analysis of community structure and succession patterns of subtidal rocky reef communities under upwelling and non-upwelling conditions in the GMR. Small-scale differences were evident depending on the oceanographic setting, but more detailed research is needed to answer the following questions:

1) How do seasonality and ENSO fluctuations affect succession and recruitment processes in tropical subtidal rocky reef communities under contrasting oceanographic conditions?

2) How do the environmental parameters (nutrients, turbidity, flow, sedimentation etc.) change with decreasing gradients of upwelling to non-upwelling?

3) How does the structure of the food web differ between upwelling and non- upwelling sites/areas?

4) How does grazer diversity affect benthic communities in contrasting environments in the GMR?

Moreover, investigations of the structure and dynamics of the plankton communities would improve our understanding about supply and recruitment peaks at the study sites. A further taxonomical identification of sessile species, such as filamentous algae, is urgently needed to enhance our knowledge about biodiversity in the GMR and conclusively about the functional redundancy of the Galápagos system, which showed to be driven by oceanography (Brandt 2012).

This knowledge is not only needed because of a better understanding in order to apply adequate management strategies for the protection of this unique and sensitive ecosystem but also to understand how different ecological processes shape marine communities (‘model system’).

118 Synthesis

Conclusively, the here presented thesis provides first small-scale investigations on the structure of Galápagos subtidal rocky reef communities and their succession patterns in contrasting oceanographic environments. To my best knowledge, it is also the first comprehensive study on succession patterns in tropical rocky reef communities

119

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130 Acknowledgements

Acknowledgements

First, I would like to thank my supervisor Prof. Dr. Matthias Wolff, who encouraged this project idea from the very beginning. Many thanks for your advice, your continuous input and support during my two-year field stay in the Charles Darwin Foundation (CDF) and afterwards at the ZMT. I particularly thank Prof. Dr. Kai Bischof for his time and acting as a second referee.

Special thanks go to Prof. Jon Witman from Brown University, who took me to my first subtidal working trip and introduced me to the vertical wall communities of Galápagos. Thank you so much for your comments, edits and your upwelling experience.

During my stay at the CDF many people helped to realize this PhD project. Special thanks go to Stuart Banks for his support since my first day in Biomar. I further thank Roby Pepolas, Germania Granda, Adelita Cruz and Sonia Cisneros for logistical support. Los biomareños and volunteers made my stay enjoyable and my work successful. Thank you so much Diego Ruiz, Roby Pepolas, Jerson Moreno, Julio Delgado, Jenifer Suarez, Nathalia Tirado, Anna Schuhbauer, Sam Clarke, Janaí Yépez, Robert Sanzogni, Daniel Sabando, Anna Alonso and Angela Kuhn. My heartfelt thanks go to Maggi Brandt, with whom I spent many good and hard times and who made me feel at home. I also thank all of my Galapageños friends for the unforgettable and great time. Thanks go to Corina Gallardo for organizing material for my experiments and Graciela Monsalve, Cristina Paz, Malena Garcia and Susi Chamorro for housing.

I also thank the Galápagos National Park for collaboration and research permits.

In Bremen, I especially thank Friedemann Keyl for his help, introducing me to the ZMT and housing. Big thanks go to Hildegard Westphal, Ursula Selent, Uli Pint, Christina Fromm, Petra Käpnik and Ago Merico for their unconditional support and making work at the ZMT possible. I also thank Esteban, Maren, Steffi, Anita, Epi, Claire, Conny and many more for having a good time at the ZMT.

Further, I give many thanks to my “PhD buddies” Carolin Herbon, Tina Oettmeier and Eva Sonnenschein for their incredible friendship, support and proof reading.

131 Acknowledgements

I would like to thank all of my friends, especially Arian with Lou for enabling me to increase my work effort. Last but not least, my biggest thanks go to my family in Magdeburg, Cuenca and Bremen for their unconditional assistance. Very special thanks go to Bernd and Christa and most important to Max and Diego, who made everything possible.

132 Appendix

Table A1. List of species registered during the study (2009-2011) in rocky reef habitat off Floreana Island.

Tres Nº Taxonomic Group Scientific Name La Botella Cuevitas Sessile Organisms 1 Macroalgae Asparagopsis spp. x x 2 Botryocladia spp. x 3 Bryopsis spp. x x 4 Carmia spp. x 5 Caulerpa spp. 6 Codium spp. x x 7 Corallina spp. x 8 Dictyota spp. x 9 Filamentous brown algae x x 10 Filamentous green algae x x 11 Filamentous red algae x x 12 Gymnogongrus spp. x x 13 Hildenbrandia spp. x x 14 Hypnea spp. x x 15 Jania spp. x x 16 Lithothamnium spp. x x 17 Nitophyllum spp. x x 18 Padina spp. x x 19 Petalonia spp. x x 20 Peyssonnelia spp. x 21 Pocockiella spp. x x 22 Pterocladia spp. x 23 Pterosiphonia spp. x x 24 Ralfsia spp. x 25 Rhodymenia spp. x 26 Sargassum spp. 27 Schizymenia ecuadoreana x 28 Spatoglossum spp. x 29 Ulva spp. x x 30 Unidentified brown algae x 31 Unidentified red algae x x 32 Anemones Bunodosoma grandis x 33 Unidentified anemone x x 34 Ascideans/Tunicates Aplidium solidum x 35 Aplidium spp. x x 36 Ascidia spp. x x 37 Didemnum perlucidum x 38 Didemnum spp. x x 39 Eudistoma spp. x 40 Pyura cf. Haustor x x 41 Unidentified ascidian 42 Bivalves Chama spp. x 43 Isognomon recognitus x

133 Appendix

Table A1. continuation…

Tres Nº Taxonomic Group Scientific Name La Botella Cuevitas 44 Bryozoans Bugula cf. californica x x 45 Bugula neritina x x 46 Caulibugula spp. x 47 Cleidochasma porcellanum x 48 Hippoporina verrilli x x 49 Lichenopora intricata x 50 Membranipora arborescens x x 51 Rhynchozoon rostratum x x 52 Thalamoporella californica x x 53 Unidentified bryozoan x 54 Ahermatypic corals Astrangia browni x 55 Cladopsammia eguchii x 56 Oulangia bradleyi x 57 Tubastraea coccinea x 58 Black corals Antipathes galapagensis x 59 Branching corals Pocillopora spp. 60 Psammocora spp. x 61 Hermatypic corals Pavona chiriquiensis 62 Pavona clavus x 63 Pavona gigantea x 64 Porites lobata x 65 Crustaceans Megabalanus peninsularis x x 66 Cyanobacteria Cyanobacteria x x 67 Dyatoms Diatomea diatomea x x 68 Gastropods Hipponix spp. x x 69 Serpulorbis margaritaceus x x 70 Hydroids Ectopleura integra 71 Macrorhynchia philippina x 72 Obelia dichotoma x x 73 Pennaria disticha x x 74 Unidentified hydroid x x 75 Polychaetes Megalomma mushaensis x x 76 Salmacina tribranchiata x x 77 Spirobranchus giganteus x x 78 Tube worm polychaete x 80 Sponges Ciocalypta spp. x x 81 Cliona chilensis x 82 Haliclona spp. x x 83 Orange sponge x x 84 Tethya sarai 85 White sponge x Mobile macroinvertebrates 1 Sea stars Coronaster marchenus x 2 Linckia columbiae x 3 Mithrodia bradleyi x 4 Nidorellia armata x x 5 Pentaceraster cumingi x x 6 Pharia pyramidata x 7 Phataria unifascialis x x

134 Appendix

Table A1. continuation…

Tres Nº Taxonomic Group Scientific Name La Botella Cuevitas 8 Crustaceans Scyllarides astori x 9 Sea urchins Centrostephanus coronatus x x 10 Eucidaris galapagensis x x 11 Lytechinus semituberculatus 12 Gastropods Columbella haemastoma x x 13 Conus nux x 14 Conus purpurascens x 15 Hexaplex princeps x x 16 Latirus sanguineus x 17 Leucozonia tuberculata x 18 Muricopsis zeteki x x 19 Pleuroploca princeps x 20 Sea cucumbers Holothuria fuscocinerea x 21 Holothuria kefersteini x 22 Isostichopus fuscus x x Reef Fish 1 Alphestes immaculatus x 2 Anisotremus interruptus x x 3 Apogon atradorsatus x x 4 Arothron meleagris 5 Aulostomus chinensis x x 6 Bodianus diplotaenia x x 7 Bodianus eclancheri x 8 Calamus taurinus x 9 Canthigaster punctatissima x 10 Cephalopholis panamensis x x 11 Chaenopsis schmitti 12 Chromis atrilobata x x 13 Cirrhitichthys oxycephalus x x 14 Cirrhitus rivulatus x 15 Decapterus muroadsi x x 16 Dermatolepis dermatolepis x 17 Diodon holocanthus x 18 Epinephelus labriformis x x 19 Fistularia commersonii x x 20 Girella freminvillei x x 21 Haemulon scudderi 22 Halichoeres dispilus x x 23 Halichoeres nicholsi x x 24 Holacanthus passer x x 25 Hypsoblennius brevipinnis x 26 Johnrandallia nigrirostris x x 27 Labrisomus dendriticus x x 28 Lutjanus argentiventris x 29 Lutjanus viridis x 30 Microspathodon dorsalis x 31 Muraena argus x 32 Mycteroperca olfax x x 33 Myrichthys tigrinus x

135 Appendix

Table A1. continuation…

Tres Nº Taxonomic Group Scientific Name La Botella Cuevitas 34 Nicholsina denticulata x x 35 Ophioblennius steindachneri x x 36 Orthopristis forbesi x x 37 Paralabrax albomaculatus x 38 Paranthias colonus x x 39 Plagiotremus azaleus x x 40 Prionurus laticlavius x x 41 Rypticus nigripinnis x 42 Scarus ghobban x x 43 Scarus perrico 44 Scomberomorus sierra x 45 Scorpaena plumieri mystes x 46 Sectator ocyurus x 47 Semicossyphus darwini x x 48 Seriola rivuliana x x 49 Serranus psittacinus x x 50 Sphoeroides annulatus x x 51 Sphyraena idiastes x 52 Stegastes leucorus beebei x x 53 Sufflamen verres x x 54 Thalassoma lucasanum x x 55 Xenocys jessiae x 56 Zanclus cornutus x 57 Dasyatis brevis x x 58 Taeniura meyeni x 59 Heterodontus quoyi x 60 Triaenodon obesus x

136