FACULTAD DE CIENCIAS DEL MAR UNIVERSIDAD CATÓLICA DEL NORTE DOCTORADO EN BIOLOGÍA Y ECOLOGÍA APLICADA

Humans as top predators in the ocean: how mechanisms structuring shallow benthic communities are influenced by fishing

Ignacio Javier Petit Vega

Supervisors: Dr. Carlos F. Gaymer and Dr. Alan M. Friedlander

COQUIMBO, 2021

1

FACULTAD DE CIENCIAS DEL MAR UNIVERSIDAD CATÓLICA DEL NORTE DOCTORADO EN BIOLOGÍA Y ECOLOGÍA APLICADA

Humans as top predators in the ocean: how mechanisms structuring shallow benthic communities are influenced by fishing

Por: Ignacio Javier Petit Vega

Departamento Biología Marina

Fecha :

Aprobado Comisión de Calificación

______Juan Machhiavello Armengol Decano Facultad Ciencia del Mar

______Profesor Guía: Dr. Carlos F. Gaymer Profesor Guía: Dr. Alan M. Friedlander

______Dr. Jaime Aburto Dr. Rodrigo Ríos

______Dr. Ivan Hinojosa Dr. Richard Wahle

Tesis entregada como un requisito para obtener el título de Doctor en Biología y Ecología Aplicada en la Facultad de Ciencias del Mar. Universidad Católica del Norte. Sede Coquimbo.

2

2021

FACULTAD DE CIENCIAS DEL MAR UNIVERSIDAD CATÓLICA DEL NORTE DOCTORADO EN BIOLOGÍA Y ECOLOGÍA APLICADA

Departamento de Biología Marina

Humans as top predators in the ocean: how mechanisms structuring

shallow benthic communities are influenced by fishing

Actividad de Titulación presentada para optar al Título de Doctor en Biología y Ecología Aplicada

Ignacio Javier Petit Vega

Coquimbo, Marzo de 2021

3

FACULTAD DE CIENCIAS DEL MAR UNIVERSIDAD CATÓLICA DEL NORTE DOCTORADO EN BIOLOGÍA Y ECOLOGÍA APLICADA

DECLARACIÓN DEL AUTOR

Se permiten citas breves sin permiso especial de la Institución o autor, siempre y cuando se otorgue el crédito correspondiente. En cualquier otra circunstancia, se deberá solicitar permiso de la Institución o el autor.

Ignacio Javier Petit Vega

Firma

2021

4

AGRADECIMIENTOS

El desarrollo exitoso de esta tesis es, sin lugar a duda, gracias a quienes me apoyaron en los diferentes procesos de cambio que ocurrieron a lo largo de estos casi 5 años de trabajo. Por lo anterior, agradezco a mi esposa Camila, que trabajó y me acompaño en las más de cien inmersiones que significo esta tesis, por enseñarme el arte del buceo más allá que una herramienta de trabajo, por las largas conversaciones interpretando la naturaleza, y por todo el amor y tiempo que me regaló para poder terminar de escribir esta tesis en tiempos de pandemia. A mi hija Maite, por compartir su vida conmigo, y es a quién tengo el placer de dedicar esta tesis, ojalá, al menos lea este par de líneas en unos años más.

A mi madre, que siempre ha sido un apoyo fundamental, entregando consejos sabios y palabras de motivación y aliento cuando los procesos fueron más complejos y agotadores, además, fue quién me enseño la filosofía del respeto, curiosidad y valoración por el mundo que nos rodea, “es, pero no es”. A mis hermanos, Eric, Titi, Rena, y Alfre por su ayuda, empuje y compañía incondicional en innumerables ocasiones, todos son un gran ejemplo de vida para mí. Quiero agradecer infinitamente a mi padre quién me apoyo incansablemente y me enseño el valor del trabajo, la perseverancia y la responsabilidad.

A mis tutores, Dr. Carlos Gaymer y Dr. Alan Friedlander, que me permitieron desarrollar esta tesis sin ningún límite a la creatividad, por entregar su conocimiento de manera amable y desinteresada, por su simpatía y buen genio, y por transmitirme el valor del esfuerzo y la rigurosidad científica en la búsqueda de la conservación de la biodiversidad marina. También a mis colegas y compañeros de laboratorio, Dra. Naiti Morales, Dr. Germán Zapata, Dr. Kosta Stamoulis, James Herlan, Dr. Sergio Carrasco, Dr. Ivan Hinojosa, Dra. Ariadna Mecho por compartir su experiencia y por las innumerables y fructíferas conversaciones. A la comisión evaluadora por sus relevantes comentarios y contribuciones a esta tesis.

Por último, a todos los amigos isleños que contribuyeron en la logística de cada campaña de terreno y nutriéndome con el conocimiento ecológico tradicional; en especial a Loti, Michel y Mareva García y a todo el equipo del centro de buceo ORCA, a Lonto Icka, Zonki, Christian Rapu, Neils Hereveri y Boris Rapu. A todos ellos muchas gracias.

5

Table of contents LIST OF FIGURES ...... 8 LIST OF TABLES ...... 10 GENERAL ABSTRACT ...... 12 RESUMEN GENERAL ...... 15 CHAPTER 1 ...... 20 INTRODUCTION ...... 20 1.1. HUMANS, THE SUPER PREDATOR ...... 20 1.2. NEARSHORE HERBIVOROUS FISH FUNCTIONAL ROLE IN CORAL REEFS ...... 22 1.3. OVEREXPLOITATION EFFECTS ON COMPETITIVE INTERACTIONS ...... 24 1.4. FISHING EFFECTS IN PREY BEHAVIOR ...... 25 1.5. GENERAL HYPOTHESES AND OBJETIVES ...... 26 i) Humans at the top of the food web: are coastal benthic communities at Rapa Nui affected by fishing? ...... 26 ii): Territoriality by the damselfish Stegastes fasciolatus (Ogilby, 1989) in the Easter Island Ecoregion: possible effects of overfishing...... 27 iii) Depth as a key fish refuge from spearfishing at Rapa Nui: anti-predator behavior in the Pacific rudderfish (Kyphosus sandwicensis)...... 27 1.6. PUBLICATIONS ...... 28 CHAPTER 2 ...... 30 Humans at the top of the food web: are coastal benthic communities at Rapa Nui affected by fishing? ...... 30 2.1. ABSTRACT ...... 31 2.2. INTRODUCTION ...... 31 2.3. MATERIALS AND METHODS ...... 34 2.4. RESULTS ...... 43 2.5. DISCUSSION ...... 56 2.6. MANAGEMENT RECOMMENDATIONS ...... 63 2.7. AKNOWLEDGMENTS...... 64 CHAPTER 3 ...... 67

6

Territoriality by the damselfish Stegastes fasciolatus (Ogilby, 1989) in the Easter Island Ecoregion: possible effects of overfishing ...... 67 3.1. ABSTRACT ...... 68 3.2. INTRODUCTION ...... 69 3.3. MATERIAL AND METHODS ...... 71 3.4. RESULTS ...... 78 3.5. DISCUSSION ...... 88 3.6. AKNOWLEDGMENTS...... 94 CHAPTER 4 ...... 96 Depth as a key fish refuge from spearfishing at Rapa Nui: anti-predator behavior in the Pacific rudderfish (Kyphosus sandwicensis) ...... 96 4.1. ABSTRACT ...... 97 4.2. INTRODUCTION ...... 98 4.3. MATERIALS AND METHODS ...... 101 4.4. RESULTS ...... 108 4.5. DISCUSION ...... 118 4.6. MANAGEMENT RECOMMENDATIONS ...... 124 4.7. ACKNOWLEDGEMENTS ...... 125 CHAPTER 5 ...... 127 General conclusions ...... 127 6. REFERENCES ...... 131

7

LIST OF FIGURES Figure 2.1. Map of Rapa Nui showing the experimental sites and Anakena, where a preliminary experiment was deployed...... 36

Figure 2.2. Percent cover of each algal functional group observed for each treatment and study area...... 45

Figure 2.3. Successional patterns of relevant algal functional groups at Rapa Nui in the three experimental treatments...... 47

Figure 2.4. Caged treatment successional pattern at Hanga Oteo...... 48

Figure 2.5. Herbivory intensity expressed as total fish bites on algae at each site ...... 50

Figure 2.6. Mean fish biomass (t ha-1) per site, and fish trophic composition per site.. ... 52

Figure 2.7. Fish assemblage structure across sites based on CAP analyses...... 53

Figure 2.8. Principal Coordinates Ordination Analysis showing the association between sites, fishing pressure, herbivory pressure, sites benthic cover and fish abundances for the final stages of open treatments for all sites...... 55

Figure 3.1. Experimental sites at Rapa Nui and Motu Motiro Hiva Marine Park...... 73

Figure 3.2. Comparisons of Stegastes fasciolatus attacks per hour at different study sites against the mirror, and against other fishes...... 80

Figure 3.3. Assemblage of fish species attacked by Stegastes fasciolatus at each experimental site during the mirror experimental trials...... 83

Figure 3.4. Number of attacks by S. fasciolatus against the mirror and other fishes relative to the numerical abundances (ind. m-2) of dominant fish taxa...... 85

Figure 3.5. Fish assemblage structure across sites based on a Canonical Analysis of

Principal Coordinates...... 87

Figure 4.1. Experimental sites at Rapa Nui and Motu Motiro Hiva Marine Park...... 103

8

Figure 4.2. Flight initiation distances (FID) by depth strata for Kyphosus sandwicensis and

Acanthurus leucopareius...... 110

Figure 4.3. Flight initiation distances (FID) of Kyphosus sandwicensis, and Acanthurus leucopareius areas among study sites...... 112

Figure 4.4. Relative frequencies of behaviors exhibited at different depths (deep, shallow) and study areas (Rapa Nui and Motu Motiro Hiva Marine Park) by Kyphosus sandwicensis and Acanthurus leucopareius...... 115

Figure 4.5. Mean biomass (t ha-1) and density plots of size structure of Kyphosus sandwicensis at Rapa Nui shallow (5 to 10 m) and deep (30 to 45 m) strata...... 117

9

LIST OF TABLES

Table 1.1. Results of analysis of variance testing the effects of site, treatment, and the associated interaction on the percent cover of each algal functional group...... 44

Table 2.2. Results of the generalized linear mixed models fitting the effect of sites on herbivory intensity (number of bites per 100 m2) and one-way ANOVA showing differences in Acanthurus leucopareius biomass among sites...... 49

Table 2.3. Results of the GLMM, Analyses of Deviance, and post-hoc analyses testing the effects of sites on the total fish biomass and fish numerical abundance...... 51

Table 3.1. Results of generalized linear models with a Poisson distribution and log-link function testing the effect of site in the number of attacks of Stegastes fasciolatus against the mirror and fishes...... 79

Table 3.2. Linear regressions showing the temporal effect in attacks of Stegastes fasciolatus against the mirror and other fishes...... 81

Table 3.3. Summary of analysis of deviance based on the multivariate generalized linear model fitting the relationship between study area and fish species attacked by Stegastes fasciolatus...... 82

Table 3.4. Results of the generalized linear models testing the effect of numerical abundances (ind. m-2) of species attacked by Stegastes fasciolatus on attack rates against other fishes and the mirror...... 84

Table 3.5. Results of analysis of variance testing the effects of time in herbivores and top predators at each site...... 88

10

Table 4.1. Results of the generalized linear mixed models based on Gaussian distributions and log-link function models testing the effect of islands, depths, fish body length (FL), and initial chasing distance (ICD) on FID of Kyphosus sandwicensis and Acanthurus leucopareius at Rapa Nui (SRN: shallow Rapa Nui and DRN: deep Rapa Nui) and Motu

Motiro Hiva Marine Park (SMMHMP: shallow Motu Motiro Hiva Marine Park)...... 109

Table 4.2. Results of the generalized linear mixed models based on Gaussian distributions and log-link function models testing the effect of sites, depth, fish body length (FL), initial chasing distance (ICD), and the interactions of site, depth, and FL in FID of Kyphosus sandwicensis and Acanthurus leucopareius...... 110

Table 4.3. Results of analysis of deviance based on the multivariate generalized linear mixed model assessing the effect of site and depth on the types of behavior performed by

Kyphosus sandwicensis when encountering scuba divers...... 113

Table 4.4. Results of analysis of deviance based on a multivariate generalized linear mixed model assessing the effect of site and depth on Kyphosus sandwicensis biomass at Rapa

Nui...... 116

Table 4.5. Results of analysis of variance testing the effects of site and depth and their interaction on Kyphosus sandwicensis size structure at Rapa Nui...... 117

11

GENERAL ABSTRACT

Throughout history humans have been considered separated from other predators due to their disproportionate influence upon the environment. Large-scale removal of species has simplified food webs resulting in the degradation of entire ecosystems relative to their original condition. This has led to alterations of ecological interactions such as herbivory and competition, as well as in animal anti-predator behavior. Currently, fishes are the most important herbivores on shallow coral reefs, where they control algal successional processes, benthic community structure and promote coral reef resilience. Globally, many coral reef fisheries are overexploited, directly affecting the structure and function of nearshore communities.

Rapa Nui (or Easter Island) is the south-eastern most corner of the Polynesian

Triangle and along with Salas & Gómez (an uninhabited island 415 km to the east of Rapa

Nui) are one of the most isolated island-groups in the Pacific Ocean and the only two islands in the Easter Island Ecoregion. Currently, coastal marine resources at Rapa Nui are declining in their abundances, likely due to overfishing. In contrast, Salas & Gómez island, within the Motu Motiro Hiva Marine Park (MMHMP), possesses a healthy nearshore coral reef community with higher biomass of coastal fishes and top predators compared to Rapa

Nui.

Thus, the main objective of this thesis was to elucidate how fishing of coastal fishes is affecting ecological interactions such as herbivory, competition, and the behavior of fishes in the coastal reef communities of Rapa Nui and compare them with those at the

MMHMP. In 2018, three independent experiments were conducted at Rapa Nui and Salas

12

& Gómez: 1) to examine changes in the functional role of herbivorous fishes in the coastal benthic community in a gradient of fishing pressure at Rapa Nui, I used artificial underwater settlement plates with different levels of herbivore exclusion; 2) to assess how overfishing indirectly affects fish territoriality in places with dissimilar abundances of top predators, I used a “mirror experiment” to trigger territorial behavior in the damselfish Stegastes fasciolatus and quantify all intra and interspecific attacks at MMHMP and Rapa Nui; and

3) to examine the effect of spearfishing on the anti-predator behavior of the pacific rudderfish Kyphosus sandwicensis, I used the Flight Initiation Distance (FID) method to investigate and estimate the minimum distance at which an observer can approach a fish before it flees. Observations were made at depths normally accessed by free divers and deeper at Rapa Nui and the MMHMP. All experiments conducted at Rapa Nui were coupled with underwater visual censuses to describe fish assemblages at each experimental site.

Herbivorous fishes effectively controlled fleshy erect algae growth along the west and north coast of Rapa Nui. In total exclusion treatments, the green algae Codium spp. dominated settlement plates representing a possible late successional stage. Significant differences in terms of fish biomass were observed across the experimental sites, suporting a potential fishing pressure gradient at Rapa Nui.

Regarding the territoriality of S. fasciolatus, three times more damselfish attacks against a mirror were found at Rapa Nui than at MMHMP, and a similar pattern was observed for attacks against other fishes. A significant positive relationship was found between the numerical abundance of the white bar surgeonfish, Acanthurus leucopareius, and the number of attacks by S. fasciolatus against fishes, while the only positive relationship with fish attacking the mirror was the abundance of K. sandwicensis; the higher

13 territoriality found at Rapa Nui could be the result of a lack of top-down control and the consequent release of herbivorous competitors.

In relation to the rudderfish anti-predator behavior, the overall FID at MMHMP was significantly shorter compared to FID in shallow strata at Rapa Nui, but this was not different from FID in deeper depths at Rapa Nui. Kyphosus sandwicensis biomass was not different among study sites at Rapa Nui, but it was significantly higher at deeper depths.

This same pattern was observed for fish body length, indicating depth as a possible refuge from fishing at Rapa Nui.

My findings highlight the functional role of coastal herbivorous fishes in controlling algae growth in the shallow benthic community of Rapa Nui and how overfishing can indirectly affect ecological interactions such as fish territoriality, as well as prey anti- predator behavior at Rapa Nui. The results of this study can help to support spatial and temporal management strategies to increase the protection of nearshore fishes in the recently created Rapa Nui Multiple Uses Marine Protected Area.

Key Words: Rapa Nui, overfishing, coral reef, fishes, marine protected areas

14

RESUMEN GENERAL

A lo largo de la historia, los humanos han sido considerados independientemente de otros depredadores debido a su desproporcionada influencia en el medioambiente. La extracción de especies a gran escala ha simplificado las redes tróficas, resultando en la degradación de ecosistemas respecto de su estado original. Lo anterior ha llevado a la alteración de importantes interacciones ecológicas tales como la herbivoría, la competencia, así como también el comportamiento animal.

Actualmente, los peces son los herbívoros más importantes en los arrecifes coralinos costeros, dentro de los cuales controlan procesos tales como los patrones sucesionales de las algas, determinan la composición de las comunidades bentónicas, y promueven la resiliencia de los arrecifes coralinos. Globalmente, muchas pesquerías de peces de arrecife se encuentran sobreexplotadas, afectando de manera directa la estructura y funcionamiento de las comunidades costeras arrecifales.

Rapa Nui (o Isla de Pascua) es la esquina sureste del Triángulo Polinésico, y con

Salas & Gómez (una pequeña isla inhabitada ubicada a 415 km al este de Rapa Nui) son uno de los grupos de islas más remotos del océano Pacífico y las únicas islas en la

Ecorregión de Isla de Pascua. Actualmente, los recursos marinos en Rapa Nui son cada vez más escasos, probablemente por la sobrepesca. En contraste, en Salas & Gómez, donde el

Parque Marino Motu Motiro Hiva (PMMMH) fue creado, sostiene una comunidad coralina costera sana en términos de una alta biomasa de peces costeros y depredadores tope en comparación con Rapa Nui.

15

De este modo, el principal objetivo de esta tesis fue dilucidar cómo la pesca de recursos marinos costeros está afectando interacciones ecológicas como la herbivoría, la competencia, así como el comportamiento animal en los arrecifes coralinos de Rapa Nui.

Así, durante el año 2018, se desarrollaron 3 experimentos independientes en Rapa Nui y

Salas & Gómez: 1) para examinar el rol funcional de los peces herbívoros en las comunidades costeras en un gradiente de presión de pesca en Rapa Nui, se utilizaron platos de asentamiento artificiales con distintos niveles de exclusión a la herbivoría; 2) para evaluar cómo la sobrepesca afecta indirectamente la territorialidad entre los peces en hábitats con abundancias disímiles de depredadores, se realizó un experimento de “espejo” para gatillar la conducta territorial del pez damisela Stegastes fasciolatus y se cuantificaron todos los ataques intra e interespecíficos en el PMMMH y Rapa Nui; 3) para examinar el efecto de la caza submarina en la conducta anti-depredatoria de un importante pez para la cultura Rapa Nui, el pez timón Kyphosus sandwicensis, se utilizó el método de la Distancia

Inicial de Escape (DIE) para investigar y estimar la distancia mínima a la cual un observador puede acercarse a un pez antes de que este escape, a profundidades normalmente frecuentadas por cazadores submarinos apneistas y más profundas en Rapa Nui y el

PMMMH. Todas las investigaciones en Rapa Nui fueron complementadas con censos visuales submarinos para describir los ensambles de peces en cada sitio experimental.

Los peces herbívoros controlaron efectivamente el crecimiento de algas erectas a lo largo de la costa oeste y norte de Rapa Nui. En los tratamientos de exclusión total, el alga verde Codium spp. dominó los platos de asentamiento evidenciando un posible estado tardío de sucesión. Las biomasas de peces fueron significativamente diferentes entre los sitios

16 experimentales, evidenciando un posible gradiente de presión de pesca a lo largo de la costa de Rapa Nui.

Respecto del comportamiento territorial de S. fasciolatus, tres veces más ataques del pez al espejo ocurrieron en Rapa Nui respecto de PMMMH, un patrón similar fue observado respecto de los ataques contra a otros peces. Una relación significativamente positiva fue observada entre la abundancia del pez cirujano de barra blanca Acanthurus leucopareius y el número de ataques dirigidos a otros peces, mientras que la única relación positiva respecto de los ataques al espejo fue observada con la abundancia de K. sandwicensis; la mayor territorialidad encontrada en Rapa Nui podría ser el resultado de la pérdida del control trófico arriba-abajo y la consecuente liberación de los herbívoros competidores.

Por último, respecto del comportamiento anti-depredatorio de K. sandwicensis, el

DIE promedio en el PMMMH fue significativamente más corto comparado con el DIE en aguas poco profundas de Rapa Nui, sin embargo, este no fue diferente del comportamiento de escape de los peces en aguas profundas de Rapa Nui. La biomasa de K. sandwicensis no fue diferente entre los sitios de estudio en Rapa Nui, pero en general fue significativamente mayor en aguas profundas. El mismo patrón fue observado para las estructuras de talla de los peces observados, indicando que la profundidad actuaría como un posible refugio ante la pesca en Rapa Nui.

Los distintos descubrimientos de esta tesis evidencian el rol funcional de los peces herbívoros como controladores de la biomasa de algas en los arrecifes someros de Rapa

Nui, y cómo la sobreexplotación pesquera afecta indirectamente las interacciones ecológicas como la territorialidad en los peces, así como su comportamiento anti-

17 depredatorio en Rapa Nui. Los resultados de este estudio pueden contribuir con información base a la propuesta de estrategias de manejo espacial y temporal para aumentar la protección efectiva del ensamble de peces costeros en la recientemente creada “Área Marina Costera

Protegida de Múltiples Usos Rapa Nui”.

Palabras claves: Rapa Nui, sobre pesca, arrecifes de coral, peces, áreas marinas protegidas

18

Chapter 1

Introduction

Photo: Camila González

19

CHAPTER 1

INTRODUCTION

1.1. HUMANS, THE SUPER PREDATOR

Humans have had a profound influence on marine ecosystems, which has resulted in trophic cascades and species extinctions (Roberts, 1995; Stallings, 2009; Terborgh and Estes, 2010;

Darimont et al., 2015). Natural communities are described to be modulated by top-down and bottom-up forces (Menge, 1992). Normally, top-down trophic cascades are generated by predator effects, such as the indirect impact that wolves have on vegetation biomass through their predation of elks (Estes et al., 2011). Conversely, bottom-up forces can influence higher trophic levels. For example, lower trophic levels (e.g. algae) can be nutritionally enriched or physiologically stressed in the presence of predators (e.g. sea snails) (Menge, 1992). However, top-down forcing due to human predatory behavior has significantly altered natural trophic webs in a way no other natural predator does due to their unequal use of resources (Terborgh and Estes, 2010). The evolution of cooperative hunting strategies and the technological development during the Pleistocene allowed human ancestors to kill larger and more numerous preys ( Roberts et al., 2001; Surovell et al., 2005; Worm and Paine, 2016). As a result, humans are considered “super predators” since they exert a disproportionately strong influence on prey relative to non-human predators that share the same prey items (Worm, 2015). For example, humans focus their hunting on the strongest and healthiest individuals of a population compared with non- human predators, which normally focus on the weaker, sicker, older or younger individuals

(Darimont et al., 2015; Worm, 2015). Similarly, humans are considered “hyperkeystone” species that prey on keystone species and, therefore, can lead to trophic cascades (Worm

20 and Paine, 2016). These classifications are consistent with the Anthropocene because of the unprecedented influence that humans currently have on the planet (Crutzen, 2006; Terborgh and Estes, 2010; Klein et al., 2014). For example, one explanation for the large mammal extinction during the Quaternary is related to the wide dispersal of prehistoric humans, which also might have modified large portions of the world´s vegetation, creating an alternative stable state (Martin and Steadman, 1999; Roberts et al., 2001). An example from the marine environment is the current status of sea urchins as the most conspicuous herbivores coastal ecosystems worldwide, which is related to the decline of sea urchin predators due to overfishing (Steneck et al., 2017). Increases in human population and the associated increases in fishing have resulted in overexploitation of most of the world’s fisheries and in a trophic downscaling of marine ecosystems (Pauly et al., 1998; Estes et al., 2011). The ecological consequences of overexploitation in the ocean have been widely studied (Heithaus et al., 2008; Worm et al., 2009; Terborgh and Estes, 2010; Worm and

Paine, 2016,). Removing species from the food web has resulted in the degradation of marine ecosystems with respect to their original condition and disrupting community structuring mechanisms such as predation and competition (Carpenter, 1986; Friedlander and DeMartini, 2002; Burkepile and Hay, 2008; Terborgh and Estes, 2010; Ceccarelli et al., 2011; Steneck et al., 2017). This alteration is particularly true for herbivory, which is a major factor in determining the structure of coral reef communities (Lewis and Wainwright,

1985). Decreased herbivorous populations due to overfishing has modified fish assemblages resulting in lower herbivory intensity and the modification of herbivorous functional roles across reefs, wich in severe cases, has led to the overgrowth of algae in several coral reefs worldwide (Mumby, 2014).

21

1.2. NEARSHORE HERBIVOROUS FISH FUNCTIONAL ROLE IN CORAL

REEFS

Since the diversification of fishes during the early Cenozoic, herbivorous fishes have been the major herbivores of shallow coral reef environments (Steneck et al., 2017). Fishes can consume algae in a more efficient manner than other benthic herbivores (e.g., sea urchins).

They can graze three-dimensional surfaces and can move freely and quickly over the reef.

Herviborous fishes have developed unique anatomical features such as specialized guts

(i.e., longer guts with greater surface relative to carnivorous species) that allow them to maximize benefits from food intake through a better absorption of nutrients and through specialized mouthparts evolved for separation of indigestible material (Moyle and Cech,

2004; Steneck et al., 2017). Based on feeding preferences and jaw morphology, herbivorous fishes can be classified into functional feeding guilds (Green and Bellwood, 2009). One such classification scheme includes four functional guilds: scrapers, excavators, grazers, and browsers (Stamoulis et al., 2017).

Generally, abundance of herbivorous fishes is high in shallow waters and declines progressively as depth increases (Brokovich et al., 2008; Friedlander et al., 2010). This pattern is correlated with the vertical distribution of algae, which is normally higher in abundance in shallow waters and declines gradually with depth because of the decrease in light penetration (Russ, 2003). At the same time, fish species composition and abundance can vary along reefs because of changes in different habitat characteristics such as wave energy, availability of refuge and food, and fishing pressure (Friedlander and Parris, 1988;

Morrison, 1988; Fox and Bellwood, 2007), resulting in a geographical gradient of herbivorous functional roles (Morrison, 1986; Cheal et al., 2013; Edwards et al., 2013). For

22 example, areas with high abundances of herbivorous fishes typically have high rates of herbivory, which results in benthic communities dominated by grazer-resistant algae (i.e., crust or turf) that are unpalatable because of hardness or toxicity (Power et al., 1988;

Terborgh and Estes, 2010). In places where populations of herbivorous fishes are absent or have been greatly reduced, algal composition and biomass consists of faster growing and more palatable species (e.g., erect fleshy algae) (Hixon et al., 1998; Power et al., 1988). In addition, herbivores play key functions in the community structuring process in coral reefs by transporting primary production to higher trophic levels, releasing substrate for sessile organisms (e.g., coral), and mediating competition for substrate between benthic sessile organism (i.e., algae and coral) (Hixon et al., 1998; Mumby et al., 2006). Herbivores can influence algal successional processes in different ways by: 1) slowing normal successional rates mediated by herbivores that inhibit later species for the benefit of earlier species; 2) accelerating successional rates mediated by herbivores inhibiting earlier species thereby benefiting later successional species; and 3) deflecting species composition in which herbivory causes different trajectories of the community.

Algal successional processes strongly depend on the composition, abundances, and selectivity of the herbivorous species present (Clements, 1916; Connell and Saltyer, 1977;

Hixon and Brostoff, 1996). Given that fishes comprise the main portion of the herbivore guild in undisturbed reefs (Lewis and Wainwright, 1985), they influence algal succession and promote coral reef resilience against algal dominated stable states (Stamoulis et al.,

2017; Steneck et al., 2017). Nowadays, the composition and abundance of fish assemblages are strongly affected by fishing, thus algal composition could be indirectly driven by human exploitation.

23

In this thesis the first question is: Is human exploitation upon coastal herbivorous fishes causing a cascading effect on algal composition?

1.3. OVEREXPLOITATION EFFECTS ON COMPETITIVE INTERACTIONS

Overexploitation has caused fish assemblages, previously dominated by top predators, to be dominated by small herbivorous and omnivorous fishes, resulting in the weakening of top-down control in many coastal habitats worldwide (Sandin et al., 2008; Friedlander and

DeMartini, 2002; Mumby, 2014), and consequently, altering the role of ecological interactions such as predation and competition (Estes et al., 2011). This trophic downgrading process can trigger the loss of ecological interactions, which may occur well before species or assemblages involved in those interactions go extinct, resulting in a loss of ecosystem services (Jensen, 1974; Estes et al., 2011; Jordano et al., 2016). Trophic cascades caused by reduced predator pressure have been reported in a vast body of literature and wide variety of taxa. For example, the indirect impact that killer whales have on macroalgal abundance through the consumption of sea otters that prey on sea urchins, which are the main herbivore in kelp ecosystems (Estes et al., 1998). In addition, the reduction of predatory pressure may result in prey release, which in turn, can affect interactions with other prey species due to their increase in abundance (Friedlander and DeMartini, 2002;

Estes et al., 2011; Davis et al., 2017).

Predation has a major impact on competitive interactions, mainly by reducing competitor population densities and, in that way, diminishing the intensity of competition, which may facilitate species coexistence (Paine, 1966; Bertness, 1989; Chase et al., 2002).

Competitive interactions have been widely considered as one of the most important mechanisms determining the structure of ecological communities (Cody and Diamond,

24

1975; Diamond and Case, 1986; Morin, 1986; Bertness, 1989). Competition can be classified in two types: exploitation and interference (Schoener, 1974), the latter is common in territorial animals (Begon et al., 1986). When predators have been removed from the ecosystem, territoriality and other competitive interactions become much more important as prey populations increase with relaxed predation (Estes et al., 2011; Davis et al., 2017).

Therefore, the second question of this thesis is as follows:

How does the intensity of territoriality between herbivorous fishes vary in a degraded environment where the only top predators are humans respect to a healthy environment with nil human influence?

1.4. FISHING EFFECTS ON PREY BEHAVIOR

Beyond decreasing prey survival, fishing can have profound effects on prey conduct with significant changes in antipredator behavior (Kulbicki, 1998, Feary et al., 2010).

Decreasing prey encounters with predators is probably one of the most effective and simple anti-predator strategies, which, in extreme cases, may modify their habitat use (Lindfield et al., 2014). For example, in places where coastal fishing pressure is high (e.g., spearfishing), individual fishes in shallow waters respond to fishing moving to greater depths as an anti- predator strategy (Hixon and Brostoff, 1996; Lindfield et al., 2014; 2015). Fishing pressure can influence essential behaviors, such as foraging in space and time, reproductive behavior, and prey escape response, all of which depend on the risk of being captured and the cost that the prey is willing to take to complete its normal activities, as described by the

Economy Hypothesis (Ydenberg and Dill, 1986; Januchowski-Hartley et al., 2012).

Specifically, fish escape behavior may show specific responses to human fishing activity

(e.g., spearfishing) (Ydenberg and Dill, 1986). Research concerning fishes flight response

25 from fishing inside and outside protected areas has demonstrated that flight reactions occur at greater distances in areas open to fishing, and show a positive linear relation with fishing pressure (Feary et al., 2010; Januchowski-Hartley et al., 2012; 2015). Thus, fish escape reactions can be used as a proxy to examine gradients of fishing pressure in vertical and horizontal space dimensions (i.e., distance to human populations and depth), and more indirectly as an assessment of marine protected areas effectiveness (Januchowski-Hartley et al., 2012). Therefore, in places without protection from fishing, depth could be an important refuge for highly prized fishes. This poses the third question of this thesis,

Is the flight response of fishes that inhabit deeper waters in places with high fishing pressure similar to areas where fishing pressure is lower?

1.5. GENERAL HYPOTHESES AND OBJECTIVES

The overall objective of this thesis is to elucidate how fishing of coastal marine resources is affecting shallow marine communities at an isolated remote oceanic island in the southern

Pacific Ocean, as developed in the following chapters:

i) Humans at the top of the food web: are coastal benthic communities at Rapa Nui affected by fishing?

Hypothesis: Fishing pressure influences algal successional patterns at Rapa Nui.

Prediction: Cover of erect fleshy algae on the shallow reef communities of Rapa Nui increases where fishing pressure on coastal herbivorous fishes is high.

Objective: Describe how fishing pressure influences the shallow algal composition in three bays with different levels of fishing pressure at Rapa Nui.

26

ii): Territoriality by the damselfish Stegastes fasciolatus (Ogilby, 1989) in the

Easter Island Ecoregion: possible effects of overfishing.

Hypothesis: Interference competition by the damselfish Stegastes fasciolatus at Rapa Nui varies among habitats with dissimilar predator abundances.

Prediction: Number of attacks by the damselfish Stegastes fasciolatus at Rapa Nui increases in habitats where predators are scarce.

Objective: Elucidate if overexploitation influences patterns of territoriality by the territorial damselfish, Stegastes fasciolatus in Rapa Nui Island.

iii) Depth as a key fish refuge from spearfishing at Rapa Nui: anti-predator behavior in the Pacific rudderfish (Kyphosus sandwicensis).

Hypothesis: Fishing pressure affect target fish anti-predator behavior at depths frequented by spearfishers.

Prediction: Fish Flight Initiation Distance (FID) from humans is shorter at greater depths at Rapa Nui, as well as, in shallow waters at Motu Motiro Hiva Marine Park, where no fishing occurs.

General objective: Determine how fishing pressure influences target fish anti-predator behavior at depths frequented by spearfishers an not.

27

1.6. PUBLICATIONS

Each research chapter of this doctoral thesis was submitted as separate publications:

Chapter 2: Humans at the top of the food web: are coastal benthic communities at Rapa Nui affected by fishing? Submitted to: Environmental Biology of Fishes.

Chapter 3: Territoriality by the damselfish Stegastes fasciolatus (Ogilby, 1989) in the Easter Island Ecoregion: possible effects of overfishing. Submitted to: Animal Behavior.

Chapter 4: Depth as a key fish refuge from spearfishing at Rapa Nui: anti-predator behavior in the Pacific rudderfish (Kyphosus sandwicensis). Submitted to: Aquatic Conservation: Marine and Freshwater Ecosystems.

28

Chapter 2

Humans at the top of the food web: are coastal benthic communities at Rapa Nui affected by fishing?

Ignacio J. Petit, Carlos F. Gaymer, Alan M. Friedlander, Joao B. Gusmao

Photo: Camila González

29

CHAPTER 2

Humans at the top of the food web: are coastal benthic communities at Rapa Nui affected by fishing?

Ignacio J. Petit a,b*, Carlos F. Gaymera,b, Alan M. Friedlanderb,c,d, Joao B. Gusmaob

a Departamento de Biología Marina, Universidad Católica del Norte, Larrondo 1281,

Coquimbo 178000, Chile

b Millennium Nucleus for Ecology and Sustainable Management of Oceanic Islands

(ESMOI), Larrondo 1281, Coquimbo 178000, Chile

c Pristine Seas, National Geographic Society, 1145 17th St NW, Washington, DC 20036,

USA

d Hawaiʿi Institute of Marine Biology, University of Hawaiʿi, Kāneʻohe, Hawaiʻi 96744,

USA

* Corresponding author e-mail: [email protected]

30

2.1. ABSTRACT

Species overexploitation has simplified food webs worldwide, resulting in the degradation of ecosystems relative to their natural state. Currently, fishes are the most important herbivores in many shallow coral reef environments, where they control algal successional processes and promote coral reef resilience. Nowadays, Rapa Nui (Easter Island), a remote

Chilean oceanic island, is suffering a serious decline in its nearshore fish populations due to overfishing. In this study, we used artificial underwater settlement plates with different levels of herbivore exclusion, and underwater visual censuses, for eight consecutive months during 2018, to examine the functional role of herbivorous fishes in structuring the coastal benthic algal community of Rapa Nui. Fishes effectively controlled fleshy erect algae growth along the west and north coast of the island. In total exclusion treatments, Codium spp. dominated settlement plates, showing a likely late successional stage when no herbivory occurred. Significant differences in fish biomass were observed across sites, gives evidence of a possible fishing gradient. The results of this study can help to inform various spatial and temporal management strategies to increase the protection of nearshore fishes at the recently created Rapa Nui Multiple Uses Marine Protected Area.

Key words: coastal fish ecology, marine protected areas, Rapa Nui, algal cover, coral reef resilience, overfishing.

2.2. INTRODUCTION

The ecological consequences of overexploitation in the ocean have been widely reported

(Terborgh and Estes, 2010; Worm and Paine, 2016; Barneche et al., 2018; Luypaert et al.,

2020). Removing species from the food web has resulted in the degradation of marine

31 ecosystems with respect to their natural state (Burkepile and Hay, 2008; Terborgh and

Estes, 2010; Ceccarelli et al., 2011; Steneck et al., 2017). This alteration of community structure is particularly true for herbivory, which is a major process in structuring coral reef communities (Lewis and Wainwright, 1985; Burkepile and Hay 2010).

Since the diversification of fishes in the early Cenozoic, herbivorous fishes have been the major herbivores of shallow coral reef environments (Steneck et al., 2017). Fishes can consume algae in a more efficient manner than other benthic herbivores (e.g., sea urchins) (Moyle and Cech, 2004; Steneck et al., 2017). Generally, the abundance of herbivorous fishes is highest in shallow water and declines progressively as depth increases

(Brokovich et al., 2008; Friedlander et al., 2010). This pattern is correlated with the vertical distribution of algae, which are normally more abundant in shallow water and declines gradually with depth because of the decrease in light penetration (Hay, 1981). At the same time, fish species composition and abundance can vary along reefs because of changes in habitat characteristics such as wave energy, availability of refuge and food, and fishing pressure (Friedlander and Parrish, 1998; Morrison, 1986; Fox and Bellwood, 2007), resulting in a spatial gradient of herbivorous functional roles (Morrison, 1986; Cheal et al.,

2013; Edwards et al., 2013). For example, areas with high abundance of herbivorous fishes typically have high rates of herbivory and consequently, a benthic community dominated by grazer-resistant algae (e.g., crust or turf), which are unpalatable because of hardness or toxicity (Power et al., 1988; Terborgh and Estes, 2010). In places where populations of herbivorous fishes are absent or have been greatly reduced, algal composition and biomass comprise faster growing and more palatable species (e.g., erect fleshy algae) (Hixon et al.,

1998; Power et al., 1988). Herbivores can influence algal successional processes in different

32 ways. They can slow normal successional rates by inhibiting colonization by later successional species. Conversely, that can accelerate successional rates by inhibiting earlier successional species facilitating later species and change species composition (Hixon et al.,

1996).

Algal successional processes strongly depend on the composition, abundances, and selectivity of the herbivorous species present (Clements, 1916; Connell and Saltyer, 1977;

Hixon and Brostoff, 1996). The composition and abundance of fish assemblages are strongly affected by fishing, thus algal successional patterns can be indirectly driven by human exploitation. Consequently, locations with high fishing pressure should have lower herbivore abundances and in turn higher fleshy algal biomass. Therefore, a fundamental question for ecology and resource management is whether human exploitation of coastal herbivorous fishes has a cascading effect on algal successional patterns.

Rapa Nui (or Easter Island) is the south-eastern most corner of the Polynesian

Triangle and along with Salas & Gómez (an uninhabited island 415 km to the east of Rapa

Nui) are one of the most isolated island-groups in the Pacific Ocean and the only two islands occurring in the Easter Island Ecoregion (Disalvo et al., 1988; Gálvez-Larach, 2009).

Fishing in Rapa Nui is an important economic and cultural activity, which contributes greatly to the local food supply (Gaymer et al., 2013; Aburto et al., 2016). Its coastal marine resources are considered overfished, especially for many prized species (Friedlander et al.,

2013; Gaymer et al., 2013; Aburto et al., 2016). Local knowledge and recent studies have described the decline in numerous coastal fish species (Aburto et al., 2015). Top predators

(e.g., sharks, jacks, etc.) occur in very low abundances at Rapa Nui compared to Salas &

Gómez (Friedlander et al., 2013, Easton et al., 2018). Similarly, herbivores such as the

33 rudderfish (Kyphosus sandwicensis) locally known as nānue is in much lower abundance at

Rapa Nui compared to Salas & Gómez (see Disalvo et al., 2007, 2008; Friedlander et al.,

2013; Zylich et al., 2014). Owing to the importance of herbivory in the ecology and indirectly in resource management of Rapa Nui, we conducted herbivore exclusion experiments coupled with quantitative in situ surveys to determine if fishing influences coastal shallow algal communities in three bays with different fishing pressures at Rapa

Nui.

2.3. MATERIALS AND METHODS

Study site

Rapa Nui is a remote Chilean oceanic island situated along the Salas & Gómez Ridge

(Figure 2.1). The island is located approximately 3700 km from the Chilean mainland and represents the southeastern most limit of coral reefs in the Pacific (Friedlander et al., 2013).

Recent studies have shown that > 50% of the shallow benthos around Rapa Nui is covered by scleractinian (stony) corals, with < 10% macroalgae cover (Friedlander et al., 2013).

Macroalgae around Rapa Nui have an Indo-Pacific affinity, with 143 described species, and at least 14% classified as endemic (Santelices and Abbott, 1987; Santelices and Meneses,

2000; Santiañez et al., 2018). With respect to fishes, planktivores were described as the most important trophic group by weight (40%), followed by herbivores (31%), while top predators represented only 2% of total fish biomass. This low biomass of top predators at

Rapa Nui is likely the result of extensive overfishing (Friedlander et al., 2013).

Three bays (Hanga Kioʿe, Vinapu, and Hanga Oteo) were selected around Rapa Nui based upon their distance to the main town (Hanga Roa). Owing to the lack of information

34 on the extent of nearshore fishing effort around Rapa Nui, the distance from Hanga Roa was used as a proxy for fishing pressure.

35

Figure 2.1. Map of Rapa Nui showing the experimental sites (black squares) and Anakena, where a preliminary experiment was deployed. Red dot identifies Hanga Roa, the main town on the island.

Hanga Kioʿe, along the west coast of the island, is the closest of the three bays to the main

town (1.4 km) and the most accessible of all experimental sites (Figure 2.1). Hanga Roa

fishing cove (caleta), which has ~ 40 active fishing boats and 4 SCUBA diving centers, is

36

< 2 km from Hanga Kioʿe. Due to its proximity to the town and harbor, Hanga Kioʿe is easily accessible by all types of fishermen (e.g., commercial and recreational) who employ a wide variety of gears (e.g., gillnet, spearfishing, handline). There are also roads and paths, which allow a wide variety of vehicles (e.g., cars, motorcycles, bikes, and horses) to access the site.

Vinapu is located 3.6 km from Hanga Roa, along the south side of the island and is the second most accessible study site (Figure 2.1). The island’s fuel depot is located at

Vinapu, which results in active ship traffic. There is a single dirt road that accesses the bay; nevertheless, it is easily accessible by boat, walking, or horse. A wide variety of fishermen use this bay, particularly on the weekends, with spearfishing being the most used gear type

(I.J. Petit pers. obs.).

Hanga Oteo, located on the north side of the island, is the farthest (11.4 km) and most inaccessible of the study sites (Figure 2.1). There is no car access, and it is a ~ 4 hour walk or 3 hours by horse from Hanga Roa. It is less fished compared with the other sites, with greater fishing intensity observed on the weekends. Handling and spearfishing are the most common fishing activities and owing to its distance from Hanga Roa, it is primarily visited by experienced fishermen by boat. In 1999, a 348 ha Coastal Marine Protected Area

(CMPA) was decreed by the Chilean government at Hanga Oteo due to its unique relief and high level of endemic biodiversity; however, no management plan was ever developed and therefore, no conservation activities have been implemented.

All three sites also differ in wave exposure. The dominant swell at Rapa Nui comes from the southeast; thus, the west and north sides of the island are protected from wave

37 action relative to the south side (Hubbard and García, 2003). Because of its southeast location, Vinapu experiences the highest level of wave impact relative to the other two locations. However, during austral winter (June-August), swells from the north are more frequent, resulting in increased wave action at Hanga Oteo. Hanga Kioʿe is the most protected of the study sites due to its west orientation. However, large northwest swells can impact this bay during winter months.

Herbivores exclusion experiment

At each site, a total of 15, 15x15 cm ceramic tiles were used as settlement plates, divided in three treatments (i.e., open, caged, fenced), and were randomly installed at each experimental site at ~ 10 m depth to examine algal successional patterns. This depth range has been identified as the zone where major fish herbivore foraging occurs (Hixon and

Brostoff, 1996; Friedlander et al., 2013, Easton et al., 2018). For all three treatments, each plate was identified with a colored cable tie. Plates were deployed on lobe coral (Porites lobata) structures, 50-60 cm above the substrate and attached using cable ties.

Five replicates of open settlement plates were deployed to examine the total and combined effect of all types of subtidal herbivores (fishes and invertebrate) along with the settlement and successional processes. At the same time, to observe algal successional patterns without herbivore pressure, five settlement plates were completely enclosed with

1x1cm mesh cages at each site to exclude fish and invertebrate grazers (Sala and

Boudouresque, 1997). A third fenced treatment (semi-caged), with 1x1 cm mesh side fences but no top, was deployed to separate the effects of benthic herbivores (e.g., sea urchins, mollusks) from fishes. We deployed five replicates of each treatment with the hope that

38 maintain a minimum of three replicates per site after anticipated losses due to environmental hazards and/or human intervention (Friedlander and Brown, 2005; Uribe et al., 2015). A fourth treatment with a top but no side fences was deployed to eliminate fish herbivory and allow invertebrate grazing, however wave activity destroyed almost all replicates in all study sites within a month of the beginning of the study, thus, this treatment was subsequently eliminated from the experiment.

Using SCUBA, plates were checked and individually photographed monthly from

May to December 2018. Later, plate images were analyzed using “ImageJ” software for digital image analyses. The percentage of algal cover over time was quantified and species composition among the differential experimental treatments was described to the lowest possible taxonomic level.

To describe the effects of fish grazing, algal growth on plates were categorized into five different functional groups (Sala and Boudouresque, 1997): (1) Fleshy Erect Algae

(FEA, all edible and erect brown, red, and green algae covering experimental plates, including filamentous algae), (2) Chlorophyte turf (CT, all non-identified chlorophyte

(green-brown) small and flat dots covering the experimental plates), (3)

Microphythobenthos (MYB, microalgal assemblages from sediment communities composed by diverse groups such as, diatoms, dinoflagellates and cyanobacteria [Heil et al., 2004]), (4) Crustose Coralline Algae (CCA), and (5) Encrusting Non-Calcareous algae

(ENCA, brown and red crust, e.g., Peyssonnelia sp.).

39

Fish composition and abundance

To describe fish assemblage composition and abundance at each experimental site, during each visit to the treatment sites fish surveys were conducted among the settlement plate treatments. A SCUBA diver counted and estimated total lengths for all fishes encountered within three fixed-length (25 m) belt transects, with different transect widths depending on the diver’s swimming direction. At each transect, all fishes ≥ 20 cm total length (TL) were enumerated within a 4 m wide band while the diver swam-out laying the transect line

(transect area = 100 m2). All fishes < 20 cm TL were recorded within a 2 m wide band on the return swim back along the laid transect line (transect area = 50 m2) (Friedlander et al.,

2013).

Individual fishes were recorded to the lowest recognizable taxon and categorized into four trophic categories: top predator, herbivore, planktivores and secondary consumer

(DeMartini et al., 2008; Friedlander et al., 2013). Total fish length was estimated to the nearest cm and individual lengths were converted to body weight and expressed in tons per hectare (t ha-1) (Friedlander et al., 2013). Individual fish biomass was calculated using the allometric length-weight conversion: W=aTLb, where parameters a and b are constant to each species, TL is total length (mm) and W is weight (g). Length-weight parameters where obtained from FishBase (Froese and Pauly, 2011). The product of individual weight and numerical density was used to estimate biomass for each species.

Fish bite count

To estimate herbivore grazing pressure at each study site, one of the major herbivorous fishes at Rapa Nui, Acanthurus leucopareius, was used as a focal species to examine bite

40 rates. Fish bite counts were made every time the settlement experiment was monitored. A

SCUBA diver randomly selected an individual fish and followed it for 1 minute from a distance of ~ 5 m to minimize the effect of diver presence on the fishes’ normal behavior.

During that period, the diver counted every bite the fish performed on the bottom. The number of fish observed during each dive varied from 5 to 10 individuals, depending on site fish abundance and diving constraints (i.e., bottom time).

Fishing pressure

As a proxy for fishing pressure, we used the distance of each experimental site to the main populated town (Hanga Roa), following the hypothesis of a negative relationship between fishing pressure and the distance from the main fishing population (Advani et al., 2015;

Silvano et al., 2017). In addition, informal interviews with experienced fishers were used to complement this hypothesis. In that way, from higher to lower fishing pressure was as follows: Hanga Kioʿe (linear distance: 1.4 km from Hanga Roa), Vinapu (linear distance:

3.6 km from Hanga Roa), and Hanga Oteo (linear distance: 11.4 km from Hanga Roa).

Data analyses

All analyses and graphing were conducted in the R computing environment (R Core Team,

2018). The effects of site and treatment on the settlement plate’s algal functional groups cover were analyzed using a 2-way analysis of variance (ANOVA). These analyses considered only the last stages of the experiment of algal succession (last three months).

The linear model included the fixed factors site (three levels = Hanga Kioʿe, Vinapu, and

Hanga Oteo) and treatment (three levels, orthogonal to site = open, caged, and fenced), as

41 well as the interactions among them. We used Tukey's Honestly Significant Difference test

(Tukey’s HSD) to perform post-hoc pairwise comparisons when applicable.

Changes in herbivory intensity, expressed by the number of fish bites on substrate, were analyzed using generalized linear mixed models (GLMMs) and Tukey’s HSD test.

We fitted a GLMM to test the effect of different sites on fish herbivory, in which site was considered a fixed factor and month was included as a random term to control for temporal variations. The GLMM was based on a Poisson distribution and log-link function and was performed using the R package lme4 (Bates et al., 2015).

Comparisons of fish biomass (t ha-1) and numerical abundances (individuals m-2) among sites were analyzed using linear mixed models (LMMs). The assumption of normal distributions was checked using the Shapiro-Wilk test, and square root and fourth root transformations were used when appropriate. GLMMs were also used when normality could not be achieved despite transformations. The mixed-effects design of the models considered site as a fixed factor (three levels = Hanga Kioʿe, Vinapu, and Hanga Oteo), and differences across surveys were controlled by including a random effect (sampled months).

The importance of site in explaining fish biomass and numerical abundance was tested using analyses of deviance and complemented with Tukey's HSD tests when pairwise comparisons were applicable. The LMMs and GLMMs were fitted using the R package lme4 (Bates et al., 2015)

Trends in the structure of the fish assemblages were analyzed using Canonical

Analyses of Principal Coordinates (CAP). The CAP ordinations were based on Bray-Curtis distances and considered the factor site as a predictor. We constructed four separate CAP

42 ordinations to examine changes in the numerical abundance and biomass of fish species and trophic groups. The CAP ordinations were constructed using the R package vegan (Oksanen et al., 2019). A Principal Coordinates Ordination Analysis (PCoA) was used to analyze the effect of fishing pressure, herbivory pressure, algal cover, and fish abundances at each experimental site upon final stages of open treatment in the whole study area.

2.4. RESULTS

Algal functional groups cover at the end of the herbivore exclusion experiment

Fleshy Erect Algae were significantly more abundant in the caged treatment overall

(P < 0.001; Table 1.1, Figure 2.2) and was significantly more abundant at Hanga Oteo compared to the other two sites (P < 0.001). MYB varied significantly among treatments (P

< 0.001; Table 1.1, Figure 2.2) and was significantly more abundant at Hanga Oteo and

Hanga Kioʿe than at Vinapu (P < 0.001). Fenced treatments had higher cover of MYB and were significantly different from caged treatments at Hanga Oteo and Hanga Kioʿe. At

Vinapu, the caged treatment had higher cover of MYB and was significantly different from the open treatment. CT was significantly more abundant at Vinapu than the other two sites

(P < 0.001; Table 1.1, Figure 2.2), with extremely low cover of CT at Hanga Kioʿe and

Hanga Oteo regardless of treatment. A significantly lower cover of CT was recorded in the caged treatment compared with fenced and open treatments (P < 0.001). ENCA showed a significantly higher cover at Hanga Kioʿe than at Hanga Oteo (P < 0.01; Table 1.1, Figure

2.2). Open treatments at Hanga Kioʿe showed significantly higher cover of ENCA than the other two treatments (P < 0.001).

43

Table 1.1. Results of the analysis of variance testing the effects of site, treatment, and the associated interaction on the percent cover of each algal functional group. S.S.= Sum of squares, M.S.= Mean squares.

Fleshy erect algae df S.S. M.S. F P Site 2 6075 3037.41 12.15 <0.001 Treatment 2 4906 24531.83 98.15 <0.001 Site x Treatment 4 5946 1486.52 5.94 <0.001 Residuals 336 8397 249.92

Microphytobenthos df S.S. M.S. F P Site 2 21294 10646.9 11.52 <0.001 Treatment 2 11012 5505.9 6.62 <0.001 Site x Treatment 4 25541 6385.0 7.68 <0.001 Residuals 336 27934 831.4

Chlorophyte turf df S.S. M.S. F P Site 2 42287 21143.43 28.90 <0.001 Treatment 2 57104 28552.22 53.38 <0.001 Site x Treatment 4 13344 336.12 6.23 <0.001 Residuals 336 17970 534.81

Encrusting non-calcareous algae df S.S. M.S. F P Site 2 115 576.10 4.64 <0.010 Treatment 2 394 1972.39 17.52 <0.001 Site x Treatment 4 663 165.47 1.47 >0.050 Residuals 336 469 4.89

Crustose coralline algae df S.S. M.S. F P Site 2 21.43 10.67 0.20 >0.050 Treatment 2 322.32 161.15 3.26 <0.050 Site x Treatment 4 802.00 200.54 4.05 <0.001 Residuals 336 16610.51 49.43

44

Figure 2.2. Percent cover of each algal functional group observed for each treatment and study area. Box plots showing median (horizontal grey line), vertical lines show the lower and upper values within 1.5 interquartile range, boxes show the limits of the 25th and 75th percentiles, and dots indicate outliers. Different capital red letter denotes significant differences in abundance between sites, while different small letters denote significant differences in abundance between treatments (α = 0.05).

45

Descriptive analysis of successional patterns of functional groups cover during the herbivore exclusion experiment

Algal functional groups showed distinct trajectories over time and among locations (Figure

2.3). ENCA and CCA were not included in this analysis because of their low cover during the study. In fenced and caged treatments, the cover of MYB increased rapidly after the first month of the study at Hanga Oteo and Hanga Kioʿe. MYB cover at Vinapu showed a similar pattern in caged treatment but a slower rate of increase in the fenced treatment.

MYB had a negative correlation with FEA in caged treatments at all sites (R = -0.169, P

<0.05), and was among the dominant functional groups during late successional stages at all study areas and treatments. FEA cover increased rapidly over time at Hanga Kioʿe and

Hanga Oteo in the caged treatment. Vinapu showed lower cover of FEA over the study period, although an increase was also observed in the caged treatment, but with a slower rate of increase. Species such as Colpomenia sinuosa, Codium spp. (Figure 2.4), and brown filamentous algae were representative of this functional group under the caged treatment, except at Vinapu where no Colpomenia sinuosa or Codium spp. were observed. Peaks in cover of CT were observed during the initial months in the open treatment for all experimental sites. Fenced and caged treatments at Hanga Kioʿe and Hanga Oteo showed low variation in cover of CT during the experiment. Early peaks in cover of CT were

46 observed in fenced and open treatments at Vinapu, where it was the dominant functional group on plates at early and late successional stages.

Figure 2.3. Successional patterns of relevant algal functional groups at Rapa Nui in the three experimental treatments (caged, fenced, open).

47

Figure 2.4. Caged treatment successional pattern at Hanga Oteo. A) bare plate initial state,

B) brown filaments (month 1), C) brown filaments and Colpomenia sinuosa recruits (month

2), D) Colpomenia sinuosa dominating plate (month 3), E) Codium spp. dominating plate

(month 7), F) preliminary experiment in the north shore (Anakena) after 13 months of experiment, the total dominance of Codium spp. illustrates a likely final stage. Months 4,

5, 6 are not showed due to the low level of changes during that time.

Herbivory intensity (fish bite count)

A total of 232 individuals of Acanthurus leucopareius were observed during focal observations of bite rates. Significant differences were observed among sites, with Hanga

Kioʿe having significantly higher overall bite rates compared to the other two sites (P <

0.001; Table 2.2; Figure 2.5) and followed by Hanga Oteo. In terms of A. leucopareius

48 biomass, Hanga Oteo had the highest biomass, followed by Hanga Kioʿe, and Vinapu, respectively (P < 0.001, Table 2.2).

Table 2.2. Results of the generalized linear mixed models fitting the effect of sites on herbivory intensity (number of bites per 100 m2) and one-way ANOVA showing differences in Acanthurus leucopareius biomass among sites. GLMM was based on a

Poisson distribution and log-link function. S.S.= Sum of squares, M.S.= Mean squares.

Number of fish bites by site Estimate Std. Error z-value P Hanga Kio`e x Hanga Oteo -0.36 0.03 -9.72 <0.001 Hanga Kio`e x Vinapu -0.53 0.04 -11.44 <0.001

Analysis of deviance for fish biomass Chi2 df P Site 175.13 2 <0.001

Pairwise comparisons Estimate p-value Hanga Oteo x Hanga Kio`e -0.36 p<0.001 Vinapu x Hanga Kio`e -0.53 p<0.001 Vinapu x Hanga Oteo -0.16 p<0.010

A. leucopareius biomass by site df S.S. M.S. F-value P Site 2 0.19 0.09 6.10 <0.001 Residuals 185 2.94 0.01

Pairwise comparisons diff P Hanga Oteo vs Hanga Kio`e 0.04 0.060 Vinapu vs Hanga Kio`e -0.04 0.250 Vinapu vs Hanga Oteo -0.08 <0.001

49

Figure 2.5. Herbivory intensity expressed as total fish bites on algae at each site from June to December 2018. Box plots showing median (horizontal grey line), vertical lines show the lower and upper values within 1.5 interquartile range, boxes show the limits of the 25th and 75th percentiles, and dots indicate outliers.

Spatial variation in fish assemblages

Significant differences were detected in fish biomass and numerical abundance among sites

(Table 2.3). Hanga Oteo had a significant higher overall fish biomass (P < 0.05; Table 2.3,

50

Figure 2.6), followed by Vinapu, and Hanga Kioʿe, respectively. Post-hoc analyzes detected

differences in fish biomass between Hanga Oteo and Hanga Kioʿe (P < 0.05). Biomass

among trophic groups differed significantly among sites (P < 0.05; Table 2.3), but post-hoc

analyzes did not detect significant differences due to marginal overall significance. Hanga

Oteo had a significant higher numerical abundance, followed by Vinapu and Hanga Kioʿe

(P < 0.001; Table 2.3). Pairwise comparisons distinguished differences in fish numerical

abundance between Hanga Oteo and the other two experimental sites (P < 0.05; Table 2.3).

Table 2.3. Results of the GLMM, Analyses of Deviance, and post-hoc analyses testing the

effects of sites on the total fish biomass and fish numerical abundance.

Total fish biomass by site Total fish numerical abundance by site Std. Std. Estimate t-value P Estimate t-value P Error Error Hanga Kio`e x Hanga Kio`e x 0.82 0.36 2.28 <0.05 1.79 0.35 5.00 <0.001 Hanga Oteo Hanga Oteo Hanga Kio`e x Hanga Kio`e x 0.24 0.41 0.59 0.55 -0.21 0.36 -0.57 0.830 Vinapu Vinapu

Analysis of deviance Analysis of deviance Chi2 df P Chi2 df P Site 7.34 2 <0.05 Site 38.33 2 <0.001

Pairwise comparisons Pairwise comparisons Comparison Estimate P Comparison Estimate P Hanga Oteo x Hanga Hanga Oteo x Hanga Kio`e 0.82 <0.05 1.79 <0.001 Kio`e Vinapu x Hanga Kio`e 0.24 0.81 Vinapu x Hanga Kio`e -0.21 0.830 Vinapu x Hanga Oteo -0.57 0.12 Vinapu x Hanga Oteo -2.00 <0.001

51

Figure 2.6. A) Mean fish biomass (t ha-1) per site, and B) fish trophic composition per site.

Bar colors represent experimental sites, SEC = secondary consumers, H = herbivores, ZP = zooplanktivores. TP = top predators. Different small letters in panel A denote significant differences between experimental sites (α = 0.05).

The biomass-based CAP ordination on species explained ~ 18% of the total variation showing separation among sites. CAP1 explained ~14% of the variation in ordination space, which was mostly related to the higher biomass of Acanthurus leucopareius, Chysiptera rapanui, and Kyphosus sandwicensis at Hanga Oteo, and Stegastes fasciolatus at Vinapu

(Figure 2.7A). Numerical abundance of species explained ~ 22% of the total variation

(Figure 2.7B). Hanga Oteo was well separated from the other sites, which was driven by the higher numerical abundance of C. rapanui. Differences in assemblage structure between

Hanga Kioʿe and Vinapu were a result of the higher abundance of S. fasciolatus at Vinapu.

Sites were not well separated in ordination space based on trophic biomass, but

52 zooplanktivores were more closely correlated with Hanga Oteo (Figure 2.7C). For trophic groups numerical abundance, CAP 1 explained ~ 18% of total variation, with Hanga Oteo separated from the other sites mainly due to the high abundance of zooplanktivorous fishes

(Figure 2.7D).

Figure 2.7. Fish assemblage structure across sites based on CAP analyses. The four panels depict ordinations based on: (A) biomass of fish species, (B) numerical abundance of fish species, (C) biomass of fish trophic groups, and (D) numerical abundance of fish trophic

53 groups. Panels (A) and (B) only show the vectors with high correlations > 0.2. Each point represents a transect. SEC = secondary consumers, H = herbivores, ZP = zooplanktivores.

TP = top predators.

Fishing pressure, herbivory pressure, and open treatments

PCoA1 explained 61% and PCoA2 explained 12% of the variation in fish assemblage structure among sites (Figure 2.8). Hanga Oteo showed was well separated in ordination space from the other two sites. Samples from Hanga Kioʿe and Vinapu showed greater variability within and between sites, as shown by the spread and overlap between them.

Algal functional groups FEA and MYB were associated with sites at Hanga Oteo along

PCoA1, while CT and CCA were associated with Hanga Kioʿe and Vinapu at the opposite end of PCoA1. ENCA and bare plates were more closely correlated with PCoA2, and orthogonal to the other substrate types. Target fish species (e.g., Caranx lugubris and

Kyphosus sandwicensis) were more closely associated with Hanga Oteo. Non-resource fish species (e.g., Stegastes fasciolatus, Diodon holocanthus, Cantherhines dumerillii) were associated with high and medium fishing pressure sites (Figure 2.8). Benthic cover at each site was associated with PCoA1. Rock and Pocillopora spp. were opposite to dead coral and Porites lobata along PCoA1. Most algae species were associated with Hanga Oteo.

54

Figure 2.8. Principal Coordinates Ordination Analysis showing the association between sites, fishing pressure (colored symbols, red = high; yellow = mid; green = low), herbivory pressure (circle size), sites benthic cover (brown text), algae functional groups (black capital letters), and fish abundances (blue text) for the final stages of open treatments for all sites. Only taxa with correlations > 0.1 for each ordination axes were included.

55

2.5. DISCUSSION

Herbivorous fishes appear to influence the composition of algae around Rapa Nui. Caging allowed the recruitment and growth of Fleshy Erect Algae, which was completely absent in fenced and open treatments.

By the end of the present study, Codium spp. dominated the caged treatments at

Hanga Oteo, indicative of a final successional stage. Furthermore, in a preliminary experiment at Anakena Bay during 2017, all caged treatments were 100% covered by

Codium spp. after 13 months. Two species of Codium have been described for Rapa Nui,

C. pocockiae and C. spongiosum (Santelices and Abbott, 1987). However, a different and unidentified species colonized and dominated our caged settlement plates. This undescribed species of Codium has rapidly become abundant over the last 10 years at Rapa Nui, successfully proliferating along the north and west coast of the island, threatening several coral reef environments normally dominated by Porites lobata between 10 and 40 m depth

(L. García pers. obs.). This species seems to be absent along the south shore, which is consistent with our results at Vinapu, where it was absent from experimental plates.

No Codium spp. recruited in the open or fenced treatments, suggesting that herbivory is controlling Codium abundance during its early stages of colonization. At Rapa

Nui, there is no report of any fish species commonly feeding on Codium spp.; however, A. leucopareius, might be controlling Codium based on data from other locations (Burkepile and Hay, 2008). Surgeonfishes are the main herbivores in many subtidal coral reef environments, grazing mainly on epilithic algal matrices (Marshell and Mumby, 2015).

Nonetheless, Burkepile and Hay (2008) noted that Acanthurus bahianus significantly

56 controlled Codium biomass in a manipulative experiment in the Florida Keys. There was no relationship between the abundance of A. leucopareius and Codium spp. (R2 = 0.12, P =

0.10) in our study. Nevertheless, in the fenced treatment, which limited the access of benthic invertebrates (e.g., sea urchins) to our settlement plates, no Codium recruited. Therefore, herbivorous fishes might be controlling Codium population along the north and west shores, and thus contributing to maintaining a stable coral-dominated state. However, since we did not detect any recruits of Codium at Vinapu in any experimental treatment, its prevalence around the island might also be related to environmental conditions, such as wave activity, which is known to be important in structuring subtidal communities (Wernberg and

Connell, 2008; Fong and Paul, 2011; Williams et al., 2013). The southeastern shore is the most wave exposed coast of Rapa Nui (Hubbard and García, 2003). As a result, benthic communities along this coast are dominated by species capable of tolerating strong water motion, such as the corals Pocillophora spp., the sea urchin Diadema savingnyi, and bare rock habitats with low algae cover (Friedlander et al., 2013). Wave energy has been noted as one of the dominant factors affecting benthic composition at Rapa Nui (Easton et al.,

2018) and might therefore be influencing Codium spp. distribution as well.

Open and fenced treatments showed similar composition of Encrusting Non-

Calcareous Algae and Chlorophyte Turf. However, Vinapu was different because of the persistent presence of CT, which decreased in dominance at Hanga Kioʿe and Hanga Oteo due to the growth of MYB. The latter dominated fenced and open treatments at Hanga Oteo and Hanga Kioʿe. Even when MYB occurred at Vinapu, its cover was lower compared to the other sites. High wave energy is noted to affect the rate of formation and destruction of

MYB due to higher sediment dynamics (Heil et al., 2004), which might explain the

57 dominance of CT over MYB at Vinapu. It is noteworthy that MYB occurred in all treatments, with dominance in the fenced, which may be a result of sediment retention in this treatment. Nevertheless, open treatments also showed a high abundance of MYB. Heil et al. (2004) identified detritivorous animals, especially sea cucumbers, as consumers of these benthic communities. High abundances of sea cucumbers (e.g., Holothuria nobilis and H. cinarescens) have been noted at Rapa Nui (Gaymer et al., 2011, Friedlander et al.,

2013). However, they were excluded from all treatments since all plates were set above corals formations (i.e., P. lobata), and therefore out of reach from organisms that inhabit sandy bottoms such as sea cucumbers.

Herbivory-resistant algal groups mainly occurred in the open treatment. The effect of herbivory decreased the competitive dominance of FEA (e.g., Codium spp., C. sinuosa) resulting in higher abundances of ENCA (e.g., Peyssonnelia rubra, Lobophora variegata) and CT at all experimental sites. These findings highlight the functional role of herbivorous fishes at Rapa Nui by modulating algal species composition, their morphology (e.g., crustose morphotype of L. variegata), clearing space for new settlers, and decreasing the proliferation of FEA. Erect algae are described as the major competitor of corals for space, owing to their high recruitment and fast growth (Mumby et al., 2006; Newman, 2006;

Taylor and Schiele, 2010). Low herbivory, which is the common state in many reefs worldwide due to overfishing, might result in algae overgrowing corals, resulting in reduced growth rate, higher tissue death, and death of entire coral colonies (Hughes et al., 1999;

Szmant et al., 2000; Jompa and McCook, 2002). Coral reefs with low herbivore abundance, like Rapa Nui, can easily be driven to an algal dominated state. It is noteworthy that the subtidal environment around Rapa Nui experienced an environmental state shift during the

58

1980s, from one dominated by macroalgae (e.g., Sargassum and Lobophora) to a coral dominated state at present. This has been well documented in the scientific literature

(Santelices, 1987; Hubbard and García, 2003), films (e.g., 1978’s Jacques Cousteau documentary on Rapa Nui) and by local ecological knowledge (Aburto et al., 2016). In addition, during this phase shift, herbivorous fishes that were strongly associated with algal patches such as the seagrass parrotfish (Leptoscarus vaigiensis) and the endemic Rapanui nibbler (Girella nebulosa) were greatly diminished in abundance from shallow subtidal habitats (Randall and Cea, 2010). Nonetheless, both fishes have been observed at Salas &

Gómez Island (I.J. Petit pers. obs., Friedlander et al., 2013), where algae abundance is lower than at Rapa Nui (Friedlander et al., 2013; Easton et al., 2018). Low abundances of these species at Rapa Nui might also be a consequence of overfishing since both species are reported as being consumed by the Rapa Nui people in the past (Wilhelm and Hulot, 1954;

Randall and Cea, 2010).

In general, successional patterns were similar between open and fenced treatments at all experimental sites, which suggests exclusion of benthic herbivores (e.g., Diadema savignyi) in the fenced treatment did not noticeably affect algal succession in the experimental plates. CT and filamentous algae colonized settlement plates early on and were then replaced by encrusting non-calcareous algae such as P. ruba and L. variegata. In all caged treatments except at Vinapu, filamentous algae were more abundant and persistent over time, which were then partially replaced by C. sinuosa, and later by Codium spp.

Species turnover in caged treatment was more pronounced at Hanga Oteo where the dominant species markedly replaced their competitors. In contrast, several species coexisted at Hanga Kioʿe, resulting in no clear algal dominance. Vinapu showed a different

59 successional pattern, with filamentous algae increasing over time until the end of experiment. The observed differences among caged treatment are likely attributed to physical or biological conditions others than herbivory. As mentioned above, Vinapu has the highest wave activity; thus, the lower algal presence found there might be due to the high level of physical disturbance (Connell, 1978). Additionally, the higher species coexistence observed at Hanga Kioʿe compared to Hanga Oteo might be a consequence of different levels of environmental disturbances, such as wave activity, which in turn can affect the intensity of competitive interaction between organisms (Connell, 1978).

We observed herbivore pressure by the focal species, A. leucoparieus, not to scale with its biomass. Bite rates were unexpectedly highest at Hanga Kioʿe whereas biomass was greatest at Hango Oteo, the site subject to the least fishing pressure. This finding contradicts the results found in other studies that describe herbivory pressure as a direct response to fish biomass (Mumby et al., 2007; Del Río et al., 2016; Arias-González et al.,

2017). A possible explanation for this might be related to the variation in competitive interactions between herbivorous fishes because of the almost complete absence of predators at Rapa Nui (Friedlander et al., 2013). Hanga Kioʿe had the lowest biomass of predators of all study sites. Prey behavior such as foraging space and time are strongly affected by the presence of predators (Lima and Dill, 1990; Lima, 1998; Gehrt and Prange,

2006; Madin et al., 2010). Thus, prey species (e.g., herbivorous fishes) inhabiting environments with no predators might have no behavioral constraints related to predator avoidance, which might result in an intensification of herbivory pressure upon algal community, like the pattern observed at Hanga Kioʿe. Herbivorous fishes influence macroalgae abundance and their composition, leaving mostly grazer-resistant species

60

(Hixon, 2015). This pattern was observed in our PCoA analysis where the ENCA functional group was strongly associated with Hanga Kioʿe, which was the site with the highest fishing pressure and lower top predator biomass, supporting a possible cascading effect of fishing upon the shallow benthic community.

Fish biomass differed across sites suggesting a possible gradient of fishing pressure.

The farther site, Hanga Oteo, had the higher biomass and the closest (Hanga Kioʿe) the lowest. The later coincides with the pattern described by Cinner and McClanahan (2008), where a negative correlation between distance from fish marketplaces and fishing pressure was found. Even when categorizations of fishing pressure among locations is theoretically possible, small islands like Rapa Nui (app. 160 km2) might not have a fishing pressure gradient since all shores are easily and fully accessible by boat, with weather (e.g., wind and waves) being the major constraint for most places (Aguila, 2020). This is reflected in the CAP ordination that shows a low level of variance (18%) in terms of species correlations within the experimental sites. When a site is overfished, resulting in target resources depletion or scarcity, fishermen must go farther to achieve their objectives, resulting in a more homogeneous pressure of fishing across the entire fished area (Williams et al., 2008;

Advani et al., 2015; Silvano et al., 2017). Variations in fishing pressure along with other bio-physical factors (e.g., eutrophication, habitat morphology, and wave exposure) may affect fish assemblage structure (Sandin et al., 2008). Prized species like Seriola lalandi,

Pseudocaranx cheilio, and Caranx lugubris occurred only at Hanga Oteo and Vinapu. The only top predators present at Hanga Kioʿe were Aulostomus chinensis and Fistularia commersonii, both species with no commercial value.

61

Even though Vinapu is relatively close to Hanga Roa, weather condition makes this site less accessible for coastal fishing activities (at least for spearfishing). In addition, deeper water is closer to the coast in comparison to the other shores, thus these conditions may result in this location being a refuge from fishing (Januchowski-Hartley et al., 2011).

This result is consistent with Morales et al. (2019), who described a higher abundance of top predators along the south shore of Rapa Nui. Conversely, Hanga Oteo showed a persistent presence of top predators during the study, which might be related to its distance from Hanga Roa. Petroglyphs discovered along the shore near Hanga Oteo show tuna, whales, and sharks, which may signify the historical presence of these top predators at this location (Lee, 2004). This area is recognized as a special cultural site and important spearfishing spot for large jacks (e.g., C. lugubris and P. cheilio). Finally, our results from

Hanga Kioʿe are consistent with higher fishing pressure based on the observations of the lower total fish biomass. The proximity to Hanga Roa town and protection from the dominant south swell allows fishing activities such as spearfishing, gill netting, and coastal handlining to occur on a regular basis by all types of fishers. Currently, experienced spearfishers travel farther due to the low abundance of targeted fishes in the waters adjacent to Hanga Roa (I.J. Petit pers. obs.), decreasing the actual fishing pressure near to the main town, which is often referred to as “the ghost of past fishing” (Silvano et al., 2017).

Resource overexploitation is not new to Rapa Nui. Ecological and social collapse in the past triggered by the complete deforestation of the island has been well documented, although the causes are still in dispute (Diamond, 2005; Hunt and Lipo, 2006; Jarman et al., 2017; Lima, 2020). In the past, fishes were reported to comprise half of the protein consumed by the Rapanui and were in such abundance, that “fishes could be caught with

62 bare hands, holding them between your legs” (Wilhelm and Hulot, 1950; Jarman et al.,

2017). Currently, overfishing is a persistent problem and islanders are aware of it, describing a continual reduction of marine resources over the past 30 years (Aburto et al.,

2015). Catch reconstructions have shown a similar pattern, with a sustained decline in catch after artisanal landings peaked in 2000 (Zylich et al., 2014; Aburto et al., 2016). Friedlander et al. (2013) highlighted the low fish biomass and the almost complete absence of top predators around Rapa Nui, which is consistent with the results found in this study seven years later. Our surveys revealed low trophic level fishes as the most abundant component of the coastal fish assemblage from Rapa Nui. The high abundance of small sized species is probably a result of overfishing of predators, the consequence of decreased top-down control and resulting prey release, suggesting a possible trophic cascade of fishing in the coastal reef community of Rapa Nui.

2.6. MANAGEMENT RECOMMENDATIONS

Developing effective management strategies is urgently needed to protect the nearshore fish stocks of Rapa Nui. The recovery of these fish populations is critical in ensuring the fundamental ecosystem role they exert upon the coastal benthic community of Rapa Nui.

In 2018, the Chilean government and the Rapa Nui people collectively established the largest MPA in the south Pacific Ocean. Despite that signficant effort, no management strategies have been implemented to conserve ecosystem function and fish biodiversity.

Therefore, based on our findings, we recommend the following spatial and temporal management strategies to be implemented.

63

i) Establishment of a no-take area at Hanga Oteo to help recover coastal

herbivorous and predator fish populations. Herbivorous fishes effectively

controlled fleshy erect algae growth in the west and north coast of the island and

increased abundance through a no-take area could help support healthy coral

communities. Science suggests that protection of at least 30% of representative

areas is needed to conserve fish populations and ecosystem function (Zhao et

al., 2020), particularly in overfished locations.

ii) Partially or totally ban fishing activities focused on herbivorous and top predator

fishes during their reproductive seasons. More research and collection of

traditional and local ecological knowledge is needed to identify spawning

seasons, which can help informing temporal management of important prized

species (e.g., Caranx lugubris, Pseudocaranx cheilio, K. sandwisensis, among

others).

The degradation of nearshore fish and benthic communities at Rapa Nui is detrimental to the lives and livelihoods of the Rapa Nui people. The ocean is one of the main sources of subsistence and has tremendous cultural importance. Thus, the inclusion of the traditional ecological knowledge, combined with scientific knowledge is fundamental to the successful resource management of nearshore reef communities at Rapa Nui.

2.7. AKNOWLEDGMENTS

64

We would like to thank ORCA diving center for their help during the whole field period of this research, as well as, to Jose Tuki and Lonto Hereveri. To C. González, A. González, C.

Robles, P. Averil, L. García for their help in different diving expeditions. To Dr. E. Macaya and his lab crew, for helping with the algae material identification. Funding: This study was financed by the Millennium Scientific Initiative, ESMOI and The Agencia Nacional de

Investigación y Desarrollo (ANID) grant N° 21170169.

Chapter 3

65

Territoriality by the damselfish Stegastes fasciolatus (Ogilby, 1989) in the Easter Island Ecoregion: possible effects of overfishing

Ignacio J. Petit, Carlos F. Gaymer, Alan M. Friedlander, Joao B. Gusmao

Photo: Dr. Iván Hinojosa

66

CHAPTER 3

Territoriality by the damselfish Stegastes fasciolatus (Ogilby, 1989) in the Easter Island Ecoregion: possible effects of overfishing

Ignacio J. Petit a,b*, Carlos F. Gaymera,b, Alan M. Friedlanderb,c,d, Joao B. Gusmaob

a Departamento de Biología Marina, Universidad Católica del Norte, Larrondo 1281,

Coquimbo 178000, Chile

b Millennium Nucleus for Ecology and Sustainable Management of Oceanic Islands

(ESMOI), Larrondo 1281, Coquimbo 178000, Chile

c Pristine Seas, National Geographic Society, 1145 17th St NW, Washington, DC 20036,

USA

d Hawaiʿi Institute of Marine Biology, University of Hawaiʿi, Kāneʻohe, Hawaiʻi 96744,

USA

* Corresponding author e-mail: [email protected]

67

3.1. ABSTRACT

Predation and competitive interactions among animals are considered among the most important mechanisms determining the structure of ecological communities. Fishing down food webs by removing top predators can dramatically decrease top-down control of these ecosystems and can indirectly modify a wide variety of prey interactions and behaviors.

Currently, Rapa Nui (Easter Island), a remote Chilean oceanic island, is suffering a serious decline in its nearshore fish stocks due to overfishing, with top predators virtually absent.

To assess how overfishing indirectly affects ecological interactions at Rapa Nui, specifically the interference competition between territorial demersal fishes at lower trophic levels, we conducted a “mirror experiment” to trigger territorial behavior in the damselfish

Stegastes fasciolatus. To evaluate both intra- and interspecific territoriality, we concurrently registered attacks by damselfish against other fishes in the area. We coupled this experiment with quantitative in situ fish surveys at three sites at Rapa Nui and one site at the Motu Motiro Hiva Marine Park (MMHMP). Overall, Rapa Nui had three times more damselfish attacks against the mirror than at MMHMP and a similar pattern was observed for attacks against other fishes. We found a significant positive relationship between the numerical abundance of the whitebar surgeonfish Acanthurus leucopareius and the number of attacks by S. fasciolatus against other fishes, while the only positive relationship with fish attacking the mirror was with the abundance of the Pacific rudderfish (Kyphosus sandwicensis). We argue that the low abundance of top predators and the higher abundance of competiting lower level consumers at Rapa Nui was the main factor triggering the stronger territorial behavior of S. fasciolatus observed at Rapa Nui compared to MMHMP, providing evidence of the ecological role that predators can play in the maintenance of

68 mechanisms such as territorially in coastal subtidal community of the Easter Island

Ecoregion.

3.2. INTRODUCTION

Predation and competitive interactions among animals have been widely considered one of the most important mechanisms determining the structure of ecological communities (Cody and Diamond, 1975; Connell, 1983; Morin, 1986; Bertness, 1989). Poorly and unregulated resource exploitation have resulted in the degradation of these ecological interactions worldwide, causing the disruption of essential ecosystem processes (Terborgh and Estes,

2010; Estes et al., 2011). Overfishing has caused fish assemblages, which were previously dominated by top predators, to now be dominated by small herbivorous and omnivorous fishes in coral reef ecosystems worldwide (Friedlander and DeMartini, 2002; Sandin et al.,

2008; Mumby, 2014). This alteration of marine trophic structures can have dramatic effects on community structuring mechanisms such as predation and competition (Paine, 1966;

Bertness, 1989). Predation has a major impact on competitive interactions, mainly by reducing competitor population densities and, in this way, diminishing the intensity of competition (Paine, 1966; Bertness, 1989; Chase et al., 2002). For example, Paine (1966) described how the predatory sea stars Pisaster ochraceus enhanced the species richness of sessile invertebrates by preferentially preying on the dominant space competitor on rocky shorelines of the west coast of North America. Lubchenco (1978) demonstrated that the herbivorous marine snail Littorina littorea controlled the abundance and type of algae in high intertidal tide pools in New England, with the highest species diversity of algae occurring at intermediate Littorina densities. These examples show how competition responds to different levels of predation in marine communities.

69

Predation not only affects prey density directly but also indirectly by influencing prey behaviors. For example, the absence of predators may result in less time invested in vigilance and more time dedicated to other activities such as feeding or reproducing

(Huntingford, 1982; Blumstein, 2005). For example, Seghers (1976), experimentally demonstrated that fishes inhabiting areas where predators were abundant had better group skills (e.g., schooling and alertness) than those inhabiting sites with fewer predators.

Predators, together with other intrinsic and extrinsic factors, such as individual social rank, identity and density of competitors, community diversity, food availability, animal fitness, habitat complexity, among others, may affect the extent of fish prey territoriality and aggressiveness (Collias, 1944; Haley and Muller, 2002; Abrey, 2005; Hess et al., 2016).

In subtidal tropical marine environments, damselfishes (Pomacentridae) from the genus Stegastes have been widely studied due to their vigorous territorial behavior

(Fishelson and Avidor, 1974; Karino and Nakazono, 1993; Cech, 2016). Damselfishes are known for incurring in interference competition, defined as "organisms directly interacting with their competitor, preventing them from exploiting a limiting resource" (Schoener,

1974; Begon et al., 1986; Hamb, 2011). This interference competition results in small algal patches that correspond to the fish’s territory, which is used for feeding and reproductive purposes (Williams, 1979; Hixon, 1983). These territories are energetically defended from herbivores and invertivores like surgeonfishes and wrasses (Canan et al., 2011; Randall and

Cea, 2011).

In the Easter Island ecoregion (Rapa Nui and Salas & Gómez islands), only three coastal Pomacentrid species occur, including two planktivores, Chromis randalli, which is endemic, and Chrysiptera rapanui, which is abundant at Rapa Nui, but is also found at the

70

Kermadec Islands and rarely at mainland New Zealand. The only benthic Pomacentrid is the South Pacific Gregory, Stegastes fasciolatus, which is distributed throughout the islands of Oceania except Hawaii and is herbivorous (Randall and Cea, 2011). S. fasciolatus is one of the most common inshore fishes at Rapa Nui, where it inhabits shallow waters (between

1 to 15 m) and defends small territories, especially from schools of other herbivorous fishes

(Disalvo et al., 1988, Randall and Cea, 2011).

The coastal marine resources of Rapa Nui are considered overfished, with top predators nearly absent (Friedlander et al., 2013; Easton et al., 2018). Therefore, manipulative experiments are fundamental to reveal and describe variation in ecological interactions such as predation and competition in order to understand the strength of top- down control, especially in environments with comparable fish assemblages (Underwood,

2000; Madin et al., 2010). Here, we conducted a "mirror experiment" to trigger the territorial interference behavior of S. fasciolatus, and registered all attacks against other fishes, together with quantitative in situ surveys, to evaluate the hypothesis that the intensity of territoriality among individual damselfish varies across environments with and without top predators, at three experimental sites at Rapa Nui and one site at the remote fully protected Motu Motiro Hiva Marine Park (MMHMP) at Salas & Gómez Island. We predict a higher rate of attacks in places with less top-down control due to the increase abundance of competitors.

3.3. MATERIAL AND METHODS

Study sites

71

Rapa Nui (Easter Island) is a remote Chilean oceanic island situated along the Salas &

Gómez Ridge (Figure 3.1). The island is approximately 3700 km west of the Chilean continent and represents the southeastern most limit of coral reefs in the Pacific (Friedlander et al., 2013). The latter authors described that > 50% of the marine benthos around Rapa

Nui was covered by scleractinian (stony) corals. With respect to the fish assemblages, planktivores were the most important trophic group by weight (40%), followed by herbivores (31%), while top predators represented only 2% of total fish biomass. This low biomass of top predators at Rapa Nui is likely the result of overfishing (Friedlander et al.,

2013).

The Motu Motiro Hiva Marine Park (MMHMP), around Salas & Gómez (a 0.15 km2 uninhabited island, located 415 km to the east of Rapa Nui), is the first large-scale marine protected area established in Chile. The coastal marine fauna at MMHMP is similar to Rapa Nui but abundances and biomass differ sharply (Friedlander et al., 2013). At

MMHMP 43% of the total reef fish biomass is comprised of top predators such as jacks and sharks, in contrast to Rapa Nui, where they compriseose less than 2% (Friedlander et al.,

2013).

Three bays (Hanga Kioʿe, Vinapu, and Hanga Oteo) were selected around Rapa Nui based upon their distance to the main town (Hanga Roa). Owing to the lack of information on the extent of nearshore fishing efforts around Rapa Nui, the distance from Hanga Roa was used as a proxy for fishing pressure; farther places were supposed to have lower fishing pressure and, thus, higher biomass of prized fishes such as top predators (Advani et al.,

2015; Silvano et al., 2017). One experimental site was selected at MMHMP based on the proximity to the anchorage site and its greater protection from wave activity.

72

Figure 3.1. Experimental sites (black open squares) at Rapa Nui and Motu Motiro Hiva

Marine Park (MMHMP). Red dot identifies Hanga Roa, the main town in Rapa Nui.

Of the three bays at Rapa Nui, Hanga Kioʿe, along the west coast of the island, is the closest to the main town (1.4 km) and the most accessible of all experimental sites (Figure 3.1). A fishing cove (“caleta”), which has ~ 40 active fishing boats and 4 SCUBA dive centers, is

< 2 km from Hanga Kioʿe. Due to its proximity, it is easily accessible by all types of fishermen (commercial, recreational, subsistence) who employ a wide variety of gear (e.g., gillnet, spearfishing, handline). There are also roads and paths, which allow different kind of vehicles (e.g., car, motorcycle, bike, horse) to access the site.

73

Vinapu is located at 3.6 km from Hanga Roa, along the south side of the island and is the second most accessible of the study sites (Figure 3.1). The island’s fuel depot is located at this site, which results in active ship traffic. There is a single dirt road that accesses the bay; nevertheless, it is easily accessible by boat, walking, or horse. A wide variety of fishermen use this bay, particularly on the weekends, with spearfishing being the most used gear type (I.J. Petit pers. obs.).

Hanga Oteo, located on the north side of the island, is the farthest (11.4 km) and most inaccessible of the study sites (Figure 3.1). There is no vehicle access, and it is an ~ 4 hour walk or 3 hours by horse from Hanga Roa. It is less fished compared with the other sites, with greater fishing intensity observed on weekends. Handlining and spearfishing are the most common fishing activities at this site and owing to its distance from Hanga Roa, it is primarily visited by experienced fishermen by boat. In 1999, 348 ha at Hanga Oteo were decreed Coastal Marine Protected Area (CMPA) due to its unique relief and high level of endemic biodiversity; however, no management plan was ever developed and therefore, no conservation activities have been implemented.

The MMHMP site is on the southwest coast of Salas & Gómez Island. The island can only be accessed by larger vessels or oceanic sailboats due to the distance from Rapa

Nui and the Chilean continent. Because of its remoteness and its protection status, all types of fishing activity at this site are nil.

All four sites differ in wave exposure. The dominant swell at Rapa Nui comes from the southeast; thus, the west and north sides of the island are protected from wave action relative to the south side (Hubbard and García, 2003). Because of its southeast location,

74

Vinapu experiences the highest level of wave impact relative to the other two locations.

However, during Austral winter (June-August), swells coming from the north are more frequent, resulting in increased wave action at Hanga Oteo. Hanga Kioʿe is the most protected of the study sites due to its west orientation. However, large northwest swells can impact this bay during winter months. Due to its small size, all shores around Salas &

Gómez are exposed to high wave activity and wind (Friedlander et al., 2013).

Attacks by Stegastes fasciolatus against fishes and mirror experiment

A mirror experiment was conducted at 10 m depth to estimate the intensity of intra and interspecific attacks at three sites around Rapa Nui with dissimilar fishing pressures and one site at MMHMP. One trial was conducted monthly from June to December in 2018 at

Rapa Nui and twice at MMHMP during January 2017. The smaller number of experimental trials conducted at MMHMP was due to a short amount of diving time spent at the island

(i.e., only 2 days). Using SCUBA, a 40 x 40 cm crystal mirror was set inside the territory of the damselfish Stegastes fasciolatus. An underwater camera (Go Pro 4 Hero) was set 3 m apart to video-record the fish’s behavior for 45 min, the first 3 minutes of each video were discarded to reduce the diver effect of the fish`s normal behavior. Videos were analyzed, and all attacks against the mirror and other fishes were registered. As a control, the same trial was conducted but instead of a mirror, a transparent crystal was used to determine if the fish was attacking its reflection or just a strange object inside its territory.

Fish composition and abundance

To describe fish assemblage composition and abundance, fish surveys were conducted monthly at each experimental site of Rapa Nui. A SCUBA diver counted and estimated

75 lengths for all fishes encountered within three fixed-length (25 m) belt transects, with transect width varying depending on the direction of swim. At each transect, all fishes ≥ 20 cm total length (TL) were enumerated within a 4-m wide band while the diver swam-out laying the transect line (transect area = 100 m2). All fishes < 20 cm TL were recorded within a 2-m wide band on the return swim back along the laid transect line (transect area = 50 m2)

(Friedlander et al., 2013).

Individual fishes were recorded to the lowest recognizable taxon and categorized into four trophic categories: top predator, herbivore, planktivore and secondary consumer

(DeMartini et al., 2008; Sandin et al., 2008; Friedlander et al., 2013). Fish length was estimated to the nearest cm and individual total body lengths were converted to body weight and expressed in tons per hectare (t ha-1) (Friedlander et al., 2013). Individual fish biomass was calculated using the allometric length-weight conversion: W=aTLb, where the parameters a and b are species-specific constant, TL is total length (mm) and W is weight

(g). Length-weight parameters where obtained from FishBase (Froese and Pauly, 2011).

The product of individual weight and numerical density was used to estimate biomass for each species (Friedlander et al., 2013).

Data analysis

Separate analyses were conducted for attacks by Stegastes fasciolatus against the mirror and fishes. Differences in the number of attacks against the mirror among sites were analyzed using generalized linear models (GLM) using a Poisson distribution and log-link function. The site effect was tested by applying an analysis of deviance. Tukey's Honest

Significant Difference (HSD) tests were used for pairwise comparisons. Changes in the frequencies of attacks against different fish species across the sites were analyzed by fitting

76 multivariate GLMs using a Poisson distribution and log-link function using the "mvabund"

R package (Wang et al., 2012). These models were based on negative binomial distributions and considered sites as a predictor (fixed factors, four levels = Hanga Oteo, Hanga Kioʿe,

Vinapu, and MMHMP). The general effects of the predictor were tested using analysis of deviance. The Holm step-down procedure was used for multiple pairwise comparisons.

To observe any influence of seasons in S. fasciolatus territorial behavior, temporal changes of attacks were assessed by applying linear regressions, in which separate models were fitted for each site at Rapa Nui. MMHMP was not included in this analysis since we only had two consecutive data collection days at this site.

The relationship between the number of attacks (against the mirror and other fishes) and the numerical abundance of the most attacked species, based on the number of attacks received by S. fasciolatus individuals, were also analyzed using Poisson GLMs. Separate models were fitted for each species and the respective abundances were considered as a covariate. A Bonferroni correction was applied to control for Type I errors. The number of attacks against fishes and the mirror was expressed as a rate (number of attacks per hour), and the abundances of the dominant species were expressed as individuals per square meter

(ind. m2).

Fish biomass were square root-transformed for all statistical analyses to normalize distributions and homogenize variances. A Canonical Analysis of Principal Coordinates

(CAP) was used to evaluate spatial changes in fish assemblages among the three sites at

Rapa Nui. MMHMP was not included into the spatial ordination due to the highly unbalanced number of sampling between islands.

77

The effect of date on fish trophic group biomass was analyzed using a 1-way analysis of variance (ANOVA). MMHMP was not included into the fish temporal analyses since we only had two consecutive data collection days.

3.4. RESULTS

Territorial behavior of Stegastes fasciolatus

A total of seven trials were run at Hanga Oteo, six each at Hanga Kioʿe and Vinapu, and two at MMHMP. The different number of trials at each site was due to environmental constraints concerning the logistic of setting up the crystal mirror experiment underwater

(i.e., particularly during the winter season, strong currents and wave activity broke the mirror and increased the instability of the mirror structure, which scared the fishes).

Behavioral responses of S. fasciolatus attacking the mirror ranged from fish observing and evading their reflection, positioning themselves side by side in front of the mirror, ramming and evading, and biting the mirror`s borders. Most attacks against other fishes followed a common pattern, with fast and abrupt upward swimming, chasing the intruder out of their territory.

Attacks against the mirror

Significant differences were observed in the number of attacks against the mirror among study areas (P < 0.001; Table 3.1; Figure 3.2A). Hanga Oteo showed a significantly higher number of attacks compared to all other sites (Table 3.1). Vinapu had significantly higher number of attacks than Hanga Kioʿe and MMHMP (Table 3.1). No attacks occurred in the control experimental trials (using a transparent crystal instead of a mirror).

78

Attacks against fishes

The attacks against fishes varied significantly among study areas (P < 0.01; Table 3.1;

Figure 3.2B). Pairwise comparisons among sites detected a significantly higher number of

attacks at Hanga Oteo compared to MMHMP and no significant differences were detected

between Hanga Oteo and the other two Rapa Nui sites (Table 1).

Table 3.1. Results of generalized linear models with a Poisson distribution and log-link

function testing the effect of site in the number of attacks of Stegastes fasciolatus against

the mirror and fishes. Tukey’s HSD results for pairwise comparisons.

Attacks against the mirror Attacks against other fishes

Res. df Deviance P Res. df Deviance P

Study site 13 195.42 < 0.001 Study site 13 73.41 < 0.01

Pairwise comparisons Estimate Adj. P Pairwise comparisons Estimate Adj. P

Hanga Oteo vs Hanga Kioʿe 1.35 <0.001 Hanga Oteo vs Hanga Kioʿe 0.26 0.51

Hanga Oteo vs Vinapu 0.39 <0.051 Hanga Oteo vs Vinapu 0.30 0.45

Hanga Oteo vs MMHMP 1.81 <0.001 Hanga Oteo vs MMHMP 0.73 <0.05

Hanga Kioʿe vs Vinapu -0.96 <0.001 Hanga Kioʿe vs Vinapu 0.03 0.99

Hanga Kioʿe vs MMHMP 0.45 0.570 Hanga Kioʿe vs MMHMP 0.46 0.38

Vinapu vs MMHMP 1.41 <0.001 Vinapu vs MMHMP 0.42 0.49

79

Figure 3.2. Comparisons of Stegastes fasciolatus attacks per hour at different study sites

(A) against the mirror, and (B) against other fishes. Box plots showing median (horizontal grey line), vertical lines show the lower and upper values within 1.5 interquartile range, boxes show the limits of the 25th and 75th percentiles, and dots indicate outliers. Sites with the same letter are not significantly different (α = 0.05).

Temporal variation of Stegastes fasciolatus attacks

80

The only significant temporal effect in attacks against other fishes was detected at Hanga

Oteo (P < 0.01; Table 3.2), showing an increase from June (n = 0 attacks) to December (n=

22 attacks). At this site, a positive but non-significant temporal trend was also found for

attacks against the mirror.

Table 3.2. Linear regressions showing the temporal effect in attacks of Stegastes fasciolatus

against the mirror and other fishes.

Attacks against the mirror Attacks against other fishes Study site Estimate Std. Error t-value P Study site Estimate Std. Error t-value P Hanga Oteo 0.33 0.15 2.13 0.12 Hanga Oteo 0.14 0.02 5.08 <0.01 Hanga Kioʿe -0.01 0.09 -0.18 0.86 Hanga Kioʿe 0.05 0.04 1.33 0.27 Vinapu 0.17 0.20 0.83 0.46 Vinapu 0.01 0.12 -0.11 0.91

Fish species attacked by Stegastes fasciolatus

The assemblage of fishes attacked by S. fasciolatus was significantly different between

study sites (P < 0.05; Table 3.3; Figure 3.3). MMHMP was significantly different from all

sites at Rapa Nui (Table 3.3), which were not different from one another. Acanthurus

leucopareius was the most attacked species overall and was always the species triggering

farther chasing distances and more aggressive responses. This species accounted for 75%

of all attacks at Hanga Oteo, 60% at Hanga Kioʿe, and ~30% at Vinapu. The endemic

butterflyfish Chaetodon litus was the second most attacked species at Rapa Nui overall and

the most attacked at Vinapu. Neither A. leucopareius nor C. litus were attacked at MMHMP,

where attacks were mainly against the scrawled filefish (Aluterus scriptus), K.

sandwicensis, and intraspecific attacks against other S. fasciolatus, which only occurred at

81

MMHMP. The sunset wrasse Thalassoma lutescens was attacked at both islands, while

Coris debueni, an endemic wrasse, was only attacked at Rapa Nui.

Table 3.3. Summary of analysis of deviance based on the multivariate generalized linear model fitting the relationship between study area and fish species attacked by Stegastes fasciolatus. Pairwise comparisons are also shown.

Fish species attacked per site

Res. df Deviance P

Study site 12 38.95 <0.005

Pairwise comparisons Obs. stat. Adj. p-value

Hanga Kioʿe vs MMHMP 16.75 <0.04

Vinapu vs MMHMP 16.75 <0.04

Hanga Oteo vs MMHMP 13.21 <0.04

Hanga Oteo vs Vinapu 11.54 0.06

Hanga Oteo vs Hanga Kioʿe 10.50 0.06

Hanga Kioʿe vs Vinapu 4.24 0.26

82

Figure 3.3. Assemblage of fish species attacked by Stegastes fasciolatus at each experimental site during the mirror experimental trials. Sites with the same letter are not significantly different (Tukey’s HSD).

Stegastes fasciolatus attacks relative to fish abundance

Attack rates targeting the mirror were negatively correlated with A. leucoparieus abundance

(P < 0.01; Table 3.4; Figure 3.4) but positively correlated with the abundance of the rudderfish K. sandwicensis (P < 0.001; Table 3.4). Attacks rates by S. fasciolatus targeting other fishes only showed a significant positive correlation with the abundances of A. leucoparieus (P < 0.001; Table 3.4; Figure 3.4). None of the other target fish abundances showed a significant correlation with attack rates (Table 3.4).

83

Table 3.4. Results of the generalized linear models testing the effect of numerical

abundances (ind. m-2) of species attacked by Stegastes fasciolatus on attack rates against

other fishes and the mirror.

Attacks against the mirror Attacks against other fishes Species/Family Estimate z-value P Species/Family Estimate z-value P Acanthurus leucopareius -2.56 -3.66 <0.01 Acanthurus leucopareius 2.36 4.32 <0.001 Kyphosus sandwicensis 175.36 8.73 <0.001 Kyphosus sandwicensis 37.25 1.34 0.17 Chaetodon litus -0.08 -0.04 0.96 Chaetodon litus -2.65 -1.04 0.29 Labrids 0.89 0.70 0.97 Labrids 2.99 1.96 0.97

84

Figure 3.4. Number of attacks by S. fasciolatus against the mirror and other fishes relative to the numerical abundances (ind. m-2) of dominant fish taxa. Black lines indicate significant linear model fits.

85

Fish spatial ordination at Rapa Nui

The numerical abundance of fish species explained ~22% of the total variation in fish assemblage spatial ordination (Figure 3.5A). Hanga Oteo was well separated from the other sites, driven by the higher numerical abundance of the Rapanui damselfish Chrysiptera rapanui. The difference in species assemblage structure between Hanga Kioʿe and Vinapu was the result of the higher number of S. fasciolatus at Vinapu. The biomass-based CAP ordination on species (Figure 3.5B) explained ~ 18% of the total variation in fish assemblage structure. CAP1 explained >14% of the variation in ordination space, which was mostly related to the higher biomass of A. leucopareius, C. rapanui, and K. sandwisencis at Hanga Oteo, and S. fasciolatus at Vinapu. For trophic group numerical abundance (Figure 3.5C), CAP 1 explained 18% of total variation in ordination space, with

Hanga Oteo separated from the other sites due mainly to the high abundance of zooplanktivorous fishes. Sites were not well separated in ordination space based on trophic groups biomass (Figure 3.5D), but zooplanktivores appeared more associated with Hanga

Oteo.

86

Figure 3.5. Fish assemblage structure across sites based on a Canonical Analysis of

Principal Coordinates. The ordinations are based on: (A) numerical abundance of fish species, (B) biomass of fish species, (C) numerical abundance of fish trophic groups, and

(D) biomass of fish trophic groups. Panels (A) and (B) only show the vectors with high correlations with each ordination axis (species scores > 0.2). Each point represents a transect. SEC: secondary consumers, H: herbivores, ZP: zooplanktivores. TP: top predators.

Herbivore and top predator temporal biomass in Rapa Nui

No significant differences were observed in the biomass of herbivores and top predators over time (P > 0.05; Table 3.5). Nonetheless, herbivores showed a non-significant increase

87 in biomass during warm-water months (October, November, and December), specially at

Hanga Oteo.

Table 3.5. Results of analysis of variance testing the effects of time in herbivores and top predators at each site. S.S.= Sum of squares, M.S.= Mean squares.

Herbivores

df S.S. F P

Date 18 0.34 1.57 0.06

Residuals 290 3.55

Top predators

df S.S. F P

Date 14 0.15 0.88 0.58

Residuals 34 0.42

3.5. DISCUSSION

The territorial behavior of Stegastes fasciolatus, revealed by attacks against the mirror and other fishes significantly differed between islands and among study sites. At MMHMP, attacks to the mirror were three times lower than at Rapa Nui, while at Hanga Oteo attacks were more frequent than at all other experimental sites, suggesting the non-lethal effect predators have on lower trophic levels at MMHMP. In addition, attacks against other fishes, were also more frequent at Hanga Oteo compared to all other sites from both islands, which was related to the higher abundance of competitors such as A. leucopareius.

88

A significant positive linear relationship was found between the number of attacks by S. fasciolatus against fishes and A. leucopareius abundance. Randall and Cea (2010) described S. fasciolatus to be normally overwhelmed by feeding schools of this surgeonfish at Rapa Nui, which is consistent with our findings. The opposite relationships found between attacks against the mirror and fishes relative to A. leucopareius abundances may be explained by an experimental bias since all registered attacks (the mirror and fishes) occurred while the mirror experiment was running and thus the presence of A. leucopareius schools or a single individual might have attracted the interest of S. fasciolatus individuals and thus decreased their attention to the mirror.

On the other hand, a significant positive correlation was observed for K. sandwicensis abundance and attacks against the mirror; however, its abundance was always very low (< 0.01 ind.m-2) making it difficult to draw definitive conclusions. Even though some competitors of S. fasciolatus occurred in low abundances at Rapa Nui (e.g., K. sandwicensis), this type of study may be strongly sensitive to the presence of a single individual as well as to fish schools since S. fasciolatus individuals could attack a single individual competitor as many times as necessary to successfully expel the intruder from its territory. In addition, the strength of the territorial behavior could be influenced by internal and external signals such as the amount of food or eggs inside the fish territory, energy necessary to complete the aggression, fish ontogenetic development, reproductive season, closeness to conspecifics, as well as the identity and quantity of competitors and the presence of top predators (Fishelson and Avidor, 1973; Haley and Muller, 2002).

Acanthurus leucopareius was the most attacked fish at Rapa Nui, while Aluterus scriptus and K. sandwisencis were the most attacked species at MMHMP. A. leucopareius

89 is the major herbivore at Rapa Nui, whereas K. sandwicensis is the dominant herbivore at

MMHMP (Friedlander et al., 2013; Easton et al., 2018). The later may explain the higher rate of attacks against A. leucopareius at Rapa Nui and against K. sandwicensis at

MMHMP, since attacks normally are directed towards the most recurrent intruder or the closest competitor (Abrey, 2005). A noteworthy artifact of the mirror experiment was that the brightness and reflection of the mirror attracted different species of fishes inside S. fasciolatus territories, which might explain the high rate of attacks against A. scriptus. Two

A. scriptus individuals stayed for as long as ~14 minutes looking at the mirror and feeding inside the S. fasciolatus territory at MMHMP, triggering territorial attacks. Other species like Arothron meleagris, Fistularia commersonii, and Xanthichthys mento were also attracted to the mirror but had less interest in it based on the shorter time they spent around the mirror, and no attacks against these species were observed. At Rapa Nui, particularly at

Hanga Oteo, labrids were more frequently targeted by S. fasciolatus, the latter coincides with higher association of Thallassoma lutescens with Hanga Oteo observed in the species abundance CAP ordination, evidencing the threat wrasses pose to S. fasciolatus at Rapa

Nui.

In the Caribbean, Thalassoma bifasciatum feeds on the demersal eggs of different damselfish species (e.g., Stegastes leucostictus, S. diencaeous, S. leucostictus) and it has been demonstrated that its presence results in a dramatic increase in the aggressive responses of Stegastes spp. (Horne and Itzkowitz, 1995; Haley and Muller, 2002; Little et al., 2013). At Rapa Nui and Salas & Gómez, nine species from the family Labridae occur nearshore, including two from the genus Thalassoma, the sunset wrasse T. lutescens and the surge wrasse T. purpureum (Randall and Cea, 2011), with a higher abundance of these

90 small sized species at Rapa Nui compared to MMHMP (Friedlander et al., 2013). The later might explain the higher rate of attacks against labrids at Rapa Nui compared to Salas &

Gómez, evidencing a possible effect of overfishing on fish interspecific interactions given by the higher abundance of small size competitors and invertivores (S. fasciolatus´s egg predators) due to the lack of top consumer control.

Fishing down food webs by removing large piscivorous fishes and top predators may result in dramatic decreases of some ecological interactions like predation (Pauly et al., 1998: Friedlander and DeMartini, 2002; Estes et al., 2011). As a result, the relaxation of top-down control can indirectly modify a wide variety of prey interactions and behaviors

(e.g., interference competition and territoriality, reproductive and foraging behavior, etc.)

(Manding et al., 2010; Oliveira et al., 2016; Davis et al., 2017). For example, fishes in higher predator abundance sites increase their vigilance activities compared to lower predator abundance sites, where fishes are less fearful (Brown et al., 1999; Manding et al.,

2010; Davis et al., 2017). This is consistent with our findings related to the lower number of attacks against other fishes and the mirror at MMHMP where fishing pressure is nil.

The high abundance of top predators at MMHMP compared to Rapa Nui (e.g.,

Carcharhinus galapagensis, Caranx lugubris, Seriola lalandi, Pseudocaranx chilensis) might be controlling prey abundances (including herbivorous fishes), and, as a result, reducing the intensity of aggressive interactions among herbivorous fishes, which may be reflected in the lower rate of attacks against other fishes and the mirror. In contrast, top predators at Rapa Nui are extremely scarce (Friedlander et al., 2013), thus, lower predation pressure in addition to other environmental characteristics, such as food availability, size of the islands, wave activity, among others, may result in a higher abundance of herbivorous

91 fishes at Rapa Nui (Easton et al., 2018), causing a stronger territorial interaction among coastal reef fishes. Therefore, we argue that the stronger territorial behavior of S. fasciolatus found at Rapa Nui compared to MMHMP, might be a consequence of the top predators being overfished at Rapa Nui. Manipulative experiments controlling physiological and environmental factors such as fish reproductive status, food availability, and refuge as limited resources, could be useful to test this hypothesis by controlling and testing these factors that have been previously described to influence the aggressiveness behavior in other Stegastes spp.

Underwater visual censuses indicated dissimilar fish assemblages among experimental sites at Rapa Nui. A. leucoparieus and K. sandwicensis were positively associated to Hanga Oteo, while C. litus and S. fasciolatus were more closely associated to

Vinapu. The later result may explain the generally higher number of attacks against other fishes and the mirror at Hanga Oteo. Petit et al. (in preparation) described a higher biomass of herbivores and secondary consumers at Hanga Oteo, followed by Vinapu, and Hanga

Kioʿe, which is consistent with the spatial patterns of aggression against the mirror found in this study. Spatial ordination of top predators based on biomass and numerical abundances did not show clear separation among sites, thus no effect of predators upon lower trophic species behavior can be assumed. The results found at the Rapa Nui sites do not correspond with the fishing pressure gradient initially proposed in this study (based in the distance to the main town), since the farther site, Hanga Oteo, had the higher number of attacks and the closest (Hanga Kioʿe) the lowest; thus, since all sites had similar low presence of predators, attacks at Rapa Nui might be more related to competitor abundance than predators presecense.

92

No clear temporal effect was observed in S. fasciolatus territorial behavior at Vinapu and Hanga Kioʿe, but a significant positive temporal effect was detected at Hanga Oteo.

Even though no temporal variation of herbivores biomass (direct competitors) was detected, a slight increase in herbivores was observed during the beginning of the warmer-water season (i.e., November – December south hemisphere) at this site, which may explain the significant increase of attacks against fishes observed at Hanga Oteo. In addition, territorial fishes like damselfishes, usually intensify competitive interactions due to nesting care and mating (Karino and Nakazono, 1993; Cech, 2016). During our fieldwork, we observed reproductive aggregations of various fishes at Rapa Nui in spring and summer (e.g.,

Arothron meleagris, Thalassoma lutescens, Heteropriacanthus cruentatus), a time that coincides with the reproductive season described for other Stegastes species (Fishelson and

Avidor, 1974; Canan et al., 2011). However, no eggs inside S. fasciolatus territories or any other reproductive activities were observed. Thus, specific research seeking to identify the reproductive period of S. fasciolatus and its relationship with fish territorial behavior is needed to fully understand how reproductive season influences the aggressive behavior of

S. faciolatus in the Easter Island Ecoregion.

This mirror technique allowed us to study fish behavior, interpreting more extensive ecological mechanisms (e.g., trophic cascades and competition), and compare ecosystems between an uninhabited island and one with intensive fishing pressure, which is key to understand the indirect consequences of fishing on these ecological interactions (Jackson et al., 2001). Recent studies have shown the effect of overfishing on the Rapa Nui coastal fish assemblage, highlighting the almost total absence of top predators and the dominance of small size herbivorous, invertivorous, and zooplanktivorous fishes (Friedlander et al., 2013,

93

Easton et al., 2018). The present study showed a possible effect of the lack of top predators by fishing in fish territorial behavior. Recovering the nearshore fish stocks of Rapa Nui by decreasing fishing pressure especially on coastal top predators is critical to recover and ensure fundamental community structuring mechanisms such as predation and competition, which would help to conserve the coral reefs of this Pacific island.

3.6. AKNOWLEDGMENTS

We would like to thank M. Petit, C. González, L. García. A. González, J. Tuki, M. García,

N. Morales, S. Carrasco, I. Hinojosa, and ORCA diving center for their help in different steps of this study. The Comisión Nacional de Investigación Científica y Tecnológica

(CONICYT) grant N° 21170169 supported the data gathering and writing work of IPV.

This study was financed by the Chilean Millennium Initiative, ESMOI.

Chapter 4

94

Depth as a key fish refuge from spearfishing at Rapa Nui: anti-predator behavior in the Pacific rudderfish (Kyphosus sandwicensis)

Ignacio J. Petit, Carlos F. Gaymer, Alan M. Friedlander, Joao B. Gusmao

Photo: Dr. Iván Hinojosa

95

CHAPTER 4

Depth as a key fish refuge from spearfishing at Rapa Nui: anti-predator behavior in the Pacific rudderfish (Kyphosus sandwicensis)

Ignacio J. Petit a,b*, Carlos F. Gaymera,b, Alan M. Friedlanderb,c,d, Joao B. Gusmaob

a Departamento de Biología Marina, Universidad Católica del Norte, Larrondo 1281,

Coquimbo 178000, Chile

b Millennium Nucleus for Ecology and Sustainable Management of Oceanic Islands

(ESMOI), Larrondo 1281, Coquimbo 178000, Chile

c Pristine Seas, National Geographic Society, 1145 17th St NW, Washington, DC 20036,

USA

d Hawaiʿi Institute of Marine Biology, University of Hawaiʿi, Kāneʻohe, Hawaiʻi 96744,

USA

* Corresponding author e-mail: [email protected]

96

4.1. ABSTRACT

Fishing is one of the main factors influencing fish behavior. Spearfishing, a common traditional cultural activity among Pacific Islanders, has been described to strongly modify the behavior of target fish species. Rapa Nui (Easter Island), a remote Chilean oceanic island, has suffered a serious decline in its nearshore fish stocks due to overfishing and spearfishing is an increasing important activity among islanders, which has contributed to this decline. In this study, we measured the flight initiation distance (FID) of the Pacific rudderfish Kyphosus sandwicensis at depths normally accessed by free divers (10 m) and those deeper (> 35 m) at three sites around Rapa Nui and one in shallow water (10 m) at the fully protected Motu Motiro Hiva Marine Park to examine the effect of spearfishing on this culturally important fish. The overall FID at MMHMP was significantly shorter compared to FID in the shallow strata at Rapa Nui, but not different from FIDs in deeper water at Rapa Nui. The biomass of K. sandwicensis did not vary significantly among study sites at Rapa Nui but increased significantly with greater depth. We hypothesize that deeper depths are a natural refuge for K. sandwicensis from spearfishing at Rapa Nui. In 2018, the

Chilean government and the Rapa Nui people collectively established the largest marine protected area in the South Pacific Ocean. However, no management strategies have been implemented to conserve coastal ecosystem processes and fish biodiversity within this

MPA. Based on our findings, we recommend various spatial and technical management strategies to increase the conservation of nearshore fishes at this isolated Pacific Island.

97

4.2. INTRODUCTION

Fishing is one of the main factors influencing fish behavior, particularly anti-predator behavior, which are characteristic of nearshore reef fishes (Kulbicki, 1998, Lima and Dill,

1990; Feary et al., 2010). Anti-predator behavior varies based on fish life-history, habitat quality, natural predator presence, fishing pressure, and the presence of humans (e.g., spearfishers, SCUBA divers) (Januchowski-Hartley et al., 2012; Stamoulis et al., 2020).

Decreasing encounters with predators is probably one of the simplest and most effective anti-predator strategies for prey species, which, in extreme cases, may modify the prey´s spatial habitat use (Lindfield et al., 2014). Depth has been described as a refuge for fish species that are targeted by fishing (Januchowski-Hartley et al., 2012). For example, in places where coastal fishing pressure is high, the greatest impacts occur in shallow water; individuals are displaced to greater depths as a strategy to avoid human predators (e.g., spearfishing) (Hixon and Brostoff, 1996; Lindfield et al., 2014; 2015). Another key anti- predator behavior when encounters with predators are inevitable is the escape behavior, defined as “the evasion of the immediate attack of a predator” (Schall and Pianka, 1980).

The decision of when to flee depends on several factors such as the identity (i.e., species and type of predator) of the predator, food quantity and availability, distance to and quantity of shelters, and to specific fishing activities (i.e., spearfishing) (Ydenberg and Dill, 1986;

Gotanda et al., 2009; Feary et al., 2010 Januchowski-Hartley et al., 2012). Responses to spearfishing depends on the risk of being captured and the cost the prey is willing to undertake to complete their regular activities (e.g., reproduction, foraging, etc.) (Ydenberg and Dill, 1986; Januchowski-Hartley et al., 2012).

98

Many different approaches have been used to study marine animal responses to predator presence (Gaymer and Himmelman, 2008; Urriago et al., 2011; 2012). One useful method is observing animal anti-predator behavior, in which coastal reef fishes have shown specific responses to spearfishers (Januchowski-Hartley et al., 2012; Stamoulis et al.,

2020). For example, fish flight responses to spearfishers studied inside and outside marine protected areas (MPAs) demonstrated that flight reaction occurred at greater distances in areas open to fishing compared to fully no-take MPAs (Feary et al., 2010; Januchowski-

Hartley et al., 2012; 2015).

Recreational fishing is one of the most common activities in coastal zones around the world (Lloret, et al., 2008). Spearfishing has been described as a low impact fishing technique; however, several investigations have shown its detrimental effects upon nearshore reef fish populations because of its high selectivity in terms of species and size classes targeted (Frisch et al., 2012). This can affect fish assemblages through the modification of the size and age structure of target species, changes in fish assemblage composition, decreases in abundance and biomass of target species, and modifications in fish behavior (e.g., time invested in foraging behavior or reproductive activities) (Lloret, et al., 2008; Godoy et al., 2010; Lienfield et al., 2014; Stamoulis et al., 2020). In the Pacific

Islands, spearfishing is a common traditional cultural activity (Tran et al., 2016). Because of its low cost and a generally limited fishery restrictions (Godoy et al., 2010; Skinner et al., 2019), the activity is prevalent, especially in remote islands where nearshore fishing is important for subsistence and recreational purposes. This is certainly the case in Rapa Nui, one of the world most remote islands in the Pacific Ocean.

99

Rapa Nui (or Easter Island) is the south-eastern most corner of the Polynesian

Triangle and along with Salas & Gómez (an uninhabited island 415 km to the east of Rapa

Nui) are one of the most isolated island-groups in the Pacific Ocean and the only two islands in the Easter Island Ecoregion (Disalvo et al., 1988; Gálvez-Larach, 2009). Two of the largest MPAs in the South Pacific Ocean occur in this Ecoregion; the “Rapa Nui Multiple

Uses Marine Protected Area” (RNMUMPA) at Rapa Nui and the remote and fully no-take

“Motu Motiro Hiva Marine Park” (MMHMP) around Salas & Gómez Island. Despite the existence of these MPAs, overfishing is a persistent problem in Rapa Nui since no management strategies have been implemented for coastal fishing. Further, continental fishing regulations are not respected by the Rapanui people as they do not represent their local culture and traditions (Friedlander and Gaymer, 2020).

Fishing in Rapa Nui is an important economic and cultural activity, which greatly contributes to the local food supply (Gaymer et al., 2013; Aburto et al., 2017). Recent studies have described the decline in numerous reef fish species and the Rapanui have noted a continual reduction in marine resources over the past 30 years (Friedlander et al., 2013;

Aburto et al., 2017). Top predators (e.g., sharks, jacks) in Rapa Nui occur in lower abundances than at Salas & Gómez Island, and this is likely due to overfishing (Friedlander et al., 2013, Easton et al., 2018). Similarly, herbivores such as the rudderfish (Kyphosus sandwicensis), locally known as nānue, occur in much lower abundances at Rapa Nui compared to Salas & Gómez (see Disalvo et al., 1998, 2007; Friedlander et al., 2013; Zylich et al., 2014).

Nānue is the most important nearshore fisheries species for the Rapanui and has a notable cultural significance, which is evidenced by the fact that it has several secondary

100 names based on size and color patterns (Randall and Cea, 2011; Friedlander et al., 2018).

Also, it is one of the main targets for spearfishing at Rapa Nui. However, no management strategies have been implemented to ensure its conservation. Observations by local SCUBA divers indicate that fish are less scared of humans at deeper depths due to the lower spearfishing pressure compared to shallow depths, thus shorter flight responses are expected at greater depths. Thus, we posed the question: Is the flight response of nānue affected by spearfishing pressure at Rapa Nui?

4.3. MATERIALS AND METHODS

Study sites

Rapa Nui is a remote Chilean oceanic island situated along the Salas & Gómez Ridge

(Figure 4.1). The island is located approximately 3700 km from the Chilean mainland and represents the southeasternmost limit of coral reefs in the Pacific (Friedlander et al., 2013).

The latter authors determined that > 50% of the marine benthos around Rapa Nui was covered by scleractinian (stony) corals, with < 10% of macroalgal cover. Among fishes, planktivores were described as the most important trophic group by weight (40%), followed by herbivores (31%), while top predators only represented 2% of total fish biomass. This low biomass of top predators at Rapa Nui is likely the result of overfishing (Friedlander et al., 2013). Motu Motiro Hiva Marine Park (MMHMP) is the first Chilean large-scale marine protected area around Salas & Gómez, a small (0.15 km2) uninhabited island located

415 km to the east of Rapa Nui (Fisher and Norris, 1960). Fish species composition at Salas

& Gómez is similar to Rapa Nui but biomass at the former is three times bigger than at

101

Rapa Nui (Friedlander et al., 2013). Because of its remoteness, 43% of the total reef fish biomass at Salas & Gómez is composed of top predators such as jacks and sharks

(Friedlander et al., 2013).

Three sites (Motu Nui, Pirámide, and Poike) were selected around Rapa Nui based upon their distance to the main town (Hanga Roa), similar reef topography (e.g., a steep slope from 10 to 40 m in depth that is easy reachable in one dive), site accessibility, and local fishermen´s recommendations. Owing to the general lack of information on the nearshore fishing efforts around Rapa Nui, specifically related to these three sites, we used the distance to the main town and site accessibility as proxies for fishing pressure. At

MMHMP, one experimental site was selected based on sea conditions for safe diving activities.

102

Figure 4.1. Experimental sites at Rapa Nui and Motu Motiro Hiva Marine Park (black open squares). Red dot identifies Hanga Roa, the main town on Rapa Nui.

Motu Nui, a small islet at the southwest corner of the island (Figure 4.1), is located at 6.9 km from Hanga Roa, with a steep vertical wall that extends down to 80 m. The proximity to Hanga Roa and the steep geomorphology makes this site easily accessible by spearfishers of various experience levels. Additionally, it is one of the most popular tourist

SCUBA diving sites in Rapa Nui. A 200 m cliff and > 1 km of ocean separate the islet from the main island, thus only boats can access this area.

103

Pirámide, on the northwest coast of the island, is at 6.4 km from Hanga Roa (Figure

4.1). The shallower area extends down to 27 m, while the deeper reef areas extends over 45 m, which restricts fishing to more experienced freedivers. Shallower areas (~ 10 m) are at

10-min swim from the deeper reef areas. This site is also an important SCUBA diving spot for tourists.

Poike, is the farthest location from Hanga Roa (21 km) and the most inaccessible of the three study sites at Rapa Nui (Figure 4.1). It is located on the northeast corner of the island with no road access and therefore only accessible by boat. A small harbor (La

Perouse) is at 7.2 km from Poike. The reef at Poike consists of a steep slope composed of boulders for the first 10 m, while at deeper depths (> 15 m) massive coral reef formations

(Porites lobata) dominate the bottom community down to 50 m (I.J. Petit pers. obs.). The reef formation makes this location favorable for both beginner and experienced spear fishermen. However, sea conditions are often unfavorable at this site, which limits spearfishing activity. Local fishermen note that this site is known for having high fish diversity and being one of the few sites around the island in which top predators are present

(Acuña et al., 2018). Due to its remoteness and rough sea conditions, it is not frequently visited by SCUBA divers.

The study site at MMHMP is located along the southwest shore of Salas & Gómez

Island. The island has no airport and due to the distance from the nearest island (415 km from Rapa Nui), only larger ships or oceanic sailing boats can reach it. Because of its remoteness and its protection status, all types of fishing activity at this site are nil.

104

Flight Initiation Distance (FID)

To study the behavior of fishes relative to human predation threat, we used flight initiation distance (FID) to investigate and estimate the minimum distance at what a diver can approach a fish before it flees (Ydenber and Dill, 1986), at depths normally accessed by free divers (10 m) and those deeper (> 35 m). Due to diving safety requirements and the limited amount of time (only 2 diving days), only a 10 m depth stratum was sampled at

MMHMP.

At each depth strata, a SCUBA diver chose a fish (Kyphosus sandwicensis) and visually estimated its total length (TL). The diver then swam directly towards the fish at a constant speed, estimating the “initial chasing distance” when the direct swimming begins and the “distance at which the fish flees (FID)”. The behavior of the focal fish was also recorded and categorized to identify stereotyped behaviors related to human presence

(Urriago et al., 2011), such as: “avoid the diver” (i.e., the fish flees with the mere presence of the diver), “keep distance” (i.e., the fish remains calm but stays away from the diver),

“approaches” (i.e., the fish approaches the diver and stays close), “look at the diver” (i.e., the fish approaches the diver but then swims away), “swims behind the diver” (i.e., the fish follows the diver), “indifferent” (i.e., the fish is not interested in the diver). The flight behavior of the white bar surgeonfish Acanthurus leucopareius, a non-targeted species at

Rapa Nui, was also assessed as a control.

Fish composition and abundance

To estimate fish assemblage and abundance along a vertical gradient of fishing pressure at each experimental site, fish surveys were conducted at typical free diving depths (~ 10 m)

105 and beyond free diving depths (35- 45 m). A SCUBA diver counted and estimated the length of all fishes encountered along a fixed-length (25-m) belt transect, with widths varying depending on the direction of swim. At each transect, all fish ≥ 20 cm total length (TL) were counted within a 4-m wide band while the diver laid out the transect line (transect area

= 100 m2). All fishes < 20 cm TL were recorded within a 2-m wide band on the return swim back along the laid transect line (transect area = 50 m2) (Friedlander et al., 2013).

Individual fishes where recorded to the lowest recognizable taxon. Fish length was estimated to the nearest cm and individual lengths were converted to body weight and expressed in tons per hectare (t ha-1) (Friedlander et al., 2013). Individual fish biomass was calculated using the allometric length-weight conversion: W=aTLb, where parameters a and b are constant to each species, TL is total length (mm) and W is weight (g). Length-weight parameters where obtained from FishBase (Froese and Pauly, 2011). The product of individual weight and numerical density was used to estimate biomass for each species

(Friedlander et al., 2013).

Data analyses

The effects of islands (MMHMP and Rapa Nui), sites, and depth on the FID of K. sandwicensis and A. leucopareius were analyzed using generalized linear mixed models

(GLMMs) with Gaussian distributions and log-link functions. The same analysis was done for A. leucopareius but depth was not included as a factor because of the low number of individuals sampled at deep stratum. The importance of each factor in explaining fish FID was tested using analyses of deviance and complemented with Tukey's Honestly Significant

Difference test (HSD) with pairwise comparisons when applicable. Islands (Rapa Nui and

106

Salas & Gómez), sites (Motu Nui, Poike, Pirámide, and MMHMP) and depth strata (shallow and deep) were the main variables of interest in this research; however, fish body length, and initial chasing distance were also included as fixed factors in the model since they have previously been reported to influence fish escape behavior (Stamoulis et al., 2017, 2020).

Date was also included in the model as a random factor to account for its effect on FID.

We applied the manyglm routine in the R package mvabund (Wang et al., 2012) to analyze differences in K. sandwicensis behavior to divers among study areas and depths at

Rapa Nui. This analysis was based on a binomial error distribution and considered study area and depth as predictors. Analysis of deviance was also applied to test the importance of site and depth and their interaction. Following this, multiple pairwise comparisons based on Holm step-down adjusted p-values for multiple testing (Westafall and Young, 1993) were performed to compare within sites and depths.

Multivariate linear models and one-way analyses of variance (ANOVA) were applied to analyze changes in biomass and the size structure of K. sandwicensis at Rapa Nui across depths and sites. Normality was tested using the Shapiro-Wilk test. Biomass was not normally distributed and only conformed to normality following a fourth-root transformation. Furthermore, we assessed the size structure of K. sandwicensis at shallow and deep depths by plotting kernel density estimates among 5 cm size intervals.

All analyses and graphing were conducted in the R computing environment (R Core

Team, 2018).

107

4.4. RESULTS

General patterns of escape behavior

The escape behavior of K. sandwicensis was significantly different between islands (P <

0.001; Table 4.1; Figure 4.2A) and depths (P < 0.001; Table 4.1, Figure 4.2A). FID for K. sandwicensis within the shallow stratum was significantly smaller at MMHMP than at Rapa

Nui (P < 0.001; Table 4.1; Figure 4.2A) but was not significantly different from the deep stratum at Rapa Nui (P > 0.05; Table 4.1; Figure 4.2A). FID at MMHMP (142.1 ± 112.5 cm) was significantly smaller than all shallow areas at Rapa Nui (P <0.001; Table 4.2;

Figure 4.3A). In contrast, deep-Pirámide and deep-Motu Nui did not differ from MMHMP

(P > 0.05; Table 4.2), while FID at Deep-Poike was significantly greater than MMHMP (P

< 0.0001; Table 4.2). No significant differences were observed at each site at Rapa Nui between depth stratum (i.e., deep and shallow) (Table 4.2). FID for K. sandwicensis was not influenced by fish body length (P > 0.05; Table 4.2). Initial chasing distance (ICD) had a significant and positive effect on FID only for K. sandwicensis (P < 0.001; Table 4.2).

The FID was not significantly influenced by the interaction between ICD x site (P > 0.05;

Table 4.2) and ICD x depth (P > 0.05; Table 4.2).

FID of A. leucopareius, the non-target species, was not significantly different between islands (P > 0.05; Table 4.1) (P > 0.05; Table 4.1; Figure 4.2B). Among sites, at shallow-Poike showed significant differences compared to shallow-Motu Nui (P < 0.001;

Table 4.2; Figure 4.3B) and shallow-Pirámide (P < 0.05; Table 4.2; Figure 4.3B). Depth strata observations of A. leucopareius were not considered in statistical analyses since only

7 individuals were found deeper than 20 m at all sites.

108

Table 4.1. Results of the generalized linear mixed models based on Gaussian distributions

and log-link function models testing the effect of islands, depths, fish body length (FL), and

initial chasing distance (ICD) on FID of Kyphosus sandwicensis and Acanthurus

leucopareius at Rapa Nui (SRN: shallow Rapa Nui and DRN: deep Rapa Nui) and Motu

Motiro Hiva Marine Park (SMMHMP: shallow Motu Motiro Hiva Marine Park).

Kyphosus sandwicensis Acanthurus leucopareius Source Chi-square df P Source Chi-square df P Island 25.47 1 < 0.001 Island 1.79 1 0.17 Depth 10.05 1 < 0.001 ICD 1.17 1 0.27 ICD 36.17 1 < 0.001 FL 1.12 1 0.28 FL 2.02 1 0.152 Pairwise comparisons Pairwise comparison Comparison Estimate Std. Error z-ratio P Comparison Estimate Std. Error z-ratio P SRN x DRN 0.39 0.14 2.75 0.051 SRN x SMMH 0.90 0.23 3.83 < 0.001 SRN x SMMH -0.10 0.50 -0.27 0.99 SMMH x DRN -0.51 0.26 -1.94 0.20

109

Figure 4.2. Flight initiation distances (FID) by depth strata for A) Kyphosus sandwicensis and B) Acanthurus leucopareius. Box plots showing median (horizontal grey line), vertical lines show the lower and upper values within 1.5 interquartile range, boxes show the limits of the 25th and 75th percentiles, and dots indicate outliers. Sites with the same letter are not significantly different (α = 0.05). No letter was added for the deep Rapa Nui of A leucopareius since depth was not included in statistical analyses.

Table 4.2. Results of the generalized linear mixed models based on Gaussian distributions and log-link function models testing the effect of sites, depth, fish body length (FL), initial chasing distance (ICD), and the interactions of site, depth, and FL in FID of Kyphosus

110 sandwicensis and Acanthurus leucopareius. Tukey’s HSD results for pairwise comparisons

FID related to depth and site. Acronyms: SMN: shallow Motu Nui, DMN: deep Motu Nui,

SPO: shallow Poike, DPO: deep Poike, SPI: shallow Pirámide, DPI: deep Pirámide,

SMMH: shallow Motu Motiro Hiva Marine Park.

Kyphosus sandwicensis Acanthurus leucopareius Source Chi-square df P Source Chi-square df P Site 44.77 3 < 0.001 Site 32.21 3 < 0.001 Depth 6.01 1 < 0.05 ICD 0.56 1 0.45 ICD 37.11 1 < 0.001 FL 0.01 1 0.91 FL 1.93 1 0.16 Site x ICD 0.11 1 0.73 Site x Depth 7.67 2 < 0.05 Site x ICD 2.73 3 0.43 Depth x ICD 0.00 1 0.97 Pairwise comparisons Pairwise comparisons Comparisons Estimate z-ratio P Comparisons Estimate z-ratio P SMN x DMN 0.41 2.48 0.20 SMN x SPO -1.46 -4.97 < 0.001 SMN x SPO -0.13 -1.20 0.93 SMN x SPI -0.70 -2.10 0.41 SMN x DPO -0.21 -1.74 0.66 SMN x SMMH -0.53 -1.38 0.86 SMN x SPI 0.05 0.52 0.99 SPO x SPI 0.75 3.50 < 0.05 SMN x DPI 0.52 3.35 < 0.05 SPO x SMMH 0.92 2.24 0.32 SMN x SMMH 0.90 5.14 < 0.001 SPI x SMMH 0.16 0.38 0.99 DMN x SPO 0.55 3.00 0.05 DMN x DPO -0.62 -3.32 < 0.05 DMN x SPI 0.35 1.94 0.52 DMN x DPI 0.11 0.53 0.99 DMN x SMMH -0.49 -2.16 0.37 SPO x DPO -0.07 -0.52 0.99 SPO x SPI 0.19 1.44 0.83 SPO x DPI 0.66 3.80 < 0.05 SPO x SMMH 1.04 5.44 < 0.001 DPO x SPI -0.27 -1.90 0.55 DPO x DPI 0.74 4.11 < 0.001 DPO x SMMH -1.11 -5.69 < 0.001 SPI x DPI 0.47 2.69 0.12 SPI x SMMH 0.84 4.43 < 0.001 DPI x SMMH -0.37 -1.71 0.68

111

Figure 4.3. Flight initiation distances (FID) of A) Kyphosus sandwicensis, and B)

Acanthurus leucopareius areas among study sites. Box plots showing median (horizontal black line), vertical lines show standard deviation and dots indicate outliers. Upper and lower quartiles, and 5th and 95th percentiles. Sites with the same letter are not significantly different (α = 0.05). No letters were added for the deep stratus of A. leucopareius since depth was not included in statistical analyses.

112

Kyphosus sandwicensis behavioral response to divers

The behavior of K. sandwicensis towards a diver differed markedly across sites (P < 0.001;

Table 4.3; Figure 4.4A) and depths (P < 0.001; Table 4.3; Figure 4.4A). The most common behaviors were “avoid the diver” (~24 %) and “keep distance” (~34%) at Rapa Nui, while these behaviors did not occur at MMHMP. In contrast, the “approach” (~33%), “swam behind the diver” (~33%), and “look at the diver” (~33%) were the most common behaviors for K. sandwicensis at MMHMP. The “avoid the diver” behavior was always more frequent in shallow stratum compared to deep stratum in all sites at Rapa Nui. Furthermore, the

“swam behind the diver” behavior only occurred at Pirámide and Motu Nui deep stratum at

Rapa Nui (Figure 4.4A).

The behavior of A. leucopareius was predominantly “indifferent” when facing a diver at all sites except shallow-Poike and it was therefore not included in further analyses

(Figure 4.4B).

Table 4.3. Results of analysis of deviance based on the multivariate GLMM model assessing the effect of site and depth on the types of behavior performed by Kyphosus sandwicensis when encountering scuba divers. SMN: shallow Motu Nui, DMN: deep Motu

Nui, SPO: shallow Poike, DPO: deep Poike, SPI: shallow Pirámide, DPI: deep Pirámide,

SMMH: shallow Motu Motiro Hiva Marine Park.

Kyphosus sandwicensis

Source df Deviance P

Site 3 399.0 < 0.001

Depth 1 157.0 < 0.001

113

Size 1 28.5 < 0.001

Pairwise comparisons

Comparison Observed statistic P

SMN x SMMH 398.73 < 0.001

SPI x SMMH 258.35 < 0.001

SPO x SMMH 227.68 < 0.001

DPO x SMMH 175.82 < 0.001

DMN x SMN 124.02 < 0.001

DPI x SMMH 100.38 < 0.001

SMN x DPI 91.74 < 0.001

DMN x SPO 89.49 < 0.001

DMN x SPI 82.22 < 0.001

DMN x DPO 64.97 < 0.001

SPO x DPI 61.44 < 0.001

DPI x SPI 55.15 < 0.001

DMN x SMMH 52.85 < 0.001

DPO x DPI 42.39 < 0.001

SPO x SPI 22.16 <0.05

DPO x SPO 19.28 0.06

SMN x SPO 17.15 0.09

DMN x DPI 12.97 0.19

SMN x DPO 12.88 0.19

DPO x SPI 10.25 0.19

SMN x SPI 4.20 0.37

114

Figure 4.4. Relative frequencies of behaviors exhibited at different depths (deep, shallow) and study areas (Rapa Nui and Motu Motiro Hiva Marine Park) by A) Kyphosus sandwicensis and B) Acanthurus leucopareius.

Kyphosus sandwicensis biomass and size structure by depth strata

Mean biomass of K. sandwicensis was significantly higher at the deeper than at the shallow stratum (P < 0.001; Table 4.4; Figure 4.5A); however, no significant differences were observed between sites (P > 0.05; Table 4.4) nor in the interaction of depth x site (P > 0.05;

Table 4.4).

The size structure of K. sandwicensis at Rapa Nui was significantly different between depths, with larger individuals predominantly occurring at the deeper stratum (P <

0.001; Table 4.5), where nānue size classes between 35 and 45 cm were more abundant.

The shallow stratum was characterized by a wide range of size classes (from 15 to 45 cm)

115

(Figure 4.5B). No differences were observed among sites (P > 0.05; Table 4.5) or the interaction of depth x site (P > 0.05; Table 4.5).

Table 4.4. Results of analysis of deviance based on a multivariate GLMM model assessing the effect of site and depth on Kyphosus sandwicensis biomass at Rapa Nui.

Kyphosus sandwicensis

Source Chi-square df P

Site 0.08 2 0.950

Depth 12.78 1 < 0.001

Site x Depth 1.22 2 0.542

Pairwise comparisons

Comparisons Estimate z-ratio p-value

DMN x DPI 0.02 0.13 1.00

DMN x DPO 0.24 0.71 0.98

DMN x SMN 0.57 2.50 0.12

DMN x SPI 0.43 2.32 0.18

DMN x SPO 0.32 1.19 0.84

DPI x DPO 0.22 0.66 0.98

DPI x SMN 0.55 2.52 0.11

DPI x SPI 0.41 2.38 0.16

DPI x SPO 0.30 1.15 0.85

DPO x SMN 0.33 0.88 0.94

DPO x SPI 0.18 0.53 0.99

DPO x SPO 0.08 0.20 1.00

SMN x SPI -0.14 -0.59 0.99

116

SMN x SPO -0.25 -0.80 0.96

SPI x SPO -0.10 -0.37 0.99

Figure 4.5. A) Mean biomass (t ha-1) and B) density plots of size structure of Kyphosus sandwicensis at Rapa Nui shallow (5 to 10 m) and deep (30 to 45 m) strata. Fitted lines in panel b indicate kernel density estimates of the size frequencies.

Table 4.5. Results of analysis of variance testing the effects of site and depth and their interaction on Kyphosus sandwicensis size structure at Rapa Nui. S.S.=Sum of squares,

M.S.=Mean squares.

117

df S.S. M.S. F P

Site 2 95 47.55 0.18 0.830

Depth 1 3016 3016.22 11.81 <0.001

Site x depth 2 193 96.30 0.37 0.680

Residuals 324 82731 255.35

4.5. DISCUSION

The flight behavior, as shown by FID, of Kyphosus sandwicensis differed significantly between Rapa Nui and MMHMP. Nānue FID was significantly smaller at MMHMP compared to all the shallow depth stratum sites at Rapa Nui but was not different from the deep stratum at Pirámide and Motu Nui. This anti-predator behavior may be evidence of lower spearfishing pressure in deeper waters with respect to the shallow stratum at Rapa

Nui. At greater depths, fishes become less accessible to freedivers (Januchowski-Hartley et al., 2011), thus, deeper depths could be an effective natural refuge from spearfishing for nānue at Rapa Nui. In contrast, no statistical differences in A. leucopareius FID were detected between most of sites, indicative of a lower influence of spearfishing with A. leucopareius.

All shallow sites at Rapa Nui had similar FIDs for K. sandwicensis. This trend might be a consequence of a similar level of fishing pressure across sites at these depths, independent of the distance from the main town. The small size of Rapa Nui (app. 160 km2), the presence of several small harbors around the island, and the fact that all shores are easily accessible by boat, increases the fishing accesibility to all areas, with wind and sea conditions the only restriction. As a result, sites farther from Hanga Roa, might have even

118 higher levels of fishing pressure given that sites closer to town are locally depleted. When a site is overfished, fishermen must go farther to achieve their objectives resulting in a more homogeneous pressure of fishing across the entire fished area (Williams et al., 2008;

Advani et al., 2015; Silvano et al., 2017). Our results of K. sandwicensis FID are consistent with this hypothesis.

Shorter FIDs for K. sandwicensis were observed at the deep stratum at Motu Nui and Pirámide, similarly to the FID observations at MMHMP, suggesting deep refuge from fishing at these sites. In contrast, Poike was the only site were deep FID observations were larger than in the shallow stratum, and the only deep site that differed statistically from

MMHMP. In addition, it was the only site where A. leucopareius FID was significantly larger than the other study sites and depths. This area was the most inaccessible, and thus shorter FIDs were expected to occur at this site, based on the hypothesis of a negative correlation between distance to town and fishing pressure (Advani et al., 2015; Anchieta et al., 2019). Nevertheless, the FID of nānue observed at Poike suggest a higher spearfishing pressure at this site. Several spears from spearguns and other type of fishing gear were found during our dives at this site. It is noteworthy that a small harbor is relatively close to

Poike, which allows spearfishers (mostly local and experienced, I.J. Petit pers. obs.) from other locations around the island to easily access the area. Thus, as mentioned above, weather and sea conditions might be the only factors restricting access to this site.

Many factors can influence fish flight behavior to divers such as, proximity to refuges, heritable and comprehensive learning process, reproductive status, an individual’s current activity, the angle and initial distance at which the diver started the chase, or fish size (Stamoulis et al., 2017, 2020). In this study, fish size did not have a significant effect

119 on flight behavior for the species studied. In contrast, initial chasing distance had a positive significant effect on nānue escape behavior but did not have significant interaction with depth and sites.

At Rapa Nui, stories told by local divers indicate that the behavior of K. sandwicensis relative to spearfishers varies according to environmental conditions (e.g., the behavior of nānue in calm mid-water environments compared to areas with strong breaking waves). Traditional ecological knowledge in Rapa Nui highlights specific areas for fishing called “toka” in Rapanui language (Ayres, 1980). Experienced spearfishers indicate that these toka act as fish aggregation sites, providing refuge and food to fishes, where fishes have a lower escape response from human predators (Cristian Rapu. Pers. comm.).

Spearfishers take advantage of this behavior by chasing nānue into the toka, which makes it easier to catch them. Native Hawaiians recognize areas where fish are known to aggregate, which are called “koa” (Poepoe et al., 2007). Koa are focal points for fishing and resource conservation. The specific locations of koa were carefully guarded secrets by

Hawaiian families who held this knowledge. Western-trained scientists and resource managers acknowledge the existence of koa (Friedlander and Parrish, 1998) but the concept remains poorly documented in fisheries science and contemporary management of

Hawai‘i’s inshore fisheries. Thus, increased research efforts seeking to identify these aggregation areas and understand their ecology at Rapa Nui would benefit from the knowledge and experiences of native Hawaiians and other Pacific Islands, with the goal of developing management strategies that are consistent with customary resource uses at Rapa

Nui. In addition to flight behavior, we observed marked differences in K. sandwicensis behaviors between islands when SCUBA divers were present. At MMHMP, nānue

120 displayed bold behaviors in presence of divers (e.g., approached, looked at the diver, and swam behind the diver). In contrast, at Rapa Nui nānue showed more fearful behaviors (e.g., kept the distance to and avoided the diver). Interestingly, the deep stratum at Motu Nui and

Pirámide were more similar to MMHMP, which was mainly driven by the higher occurrence of “look at the diver” and “approach” behaviors. Furthermore, these where the only sites at Rapa Nui were “swam behind the diver” behavior occurred. The wider variety of nānue behaviors observed at Rapa Nui may be a strategy to reduce predation risk related to the human predator presence. In contrats, A. leucopareius behavior did not differ between islands or among sites, with a high prevalence of indifference to divers, probably explained by the lower interest A. leucopareius represents to spearfishers.

The effect of human predation on the nearshore reef fishes at Rapa Nui has resulted in the modification of fish assemblages due to overfishing (Friedlander et al., 2013; Easton et al., 2018). At MMHMP, 43% of the total fish biomass is composed by top predators such as jacks and sharks, while at Rapa Nui top predators represent only 2%, as well as, overall herbivores biomass being 3 times lower at Rapa Nui compared to MMHMP (Friedlander et al., 2013). The overall biomass of nānue at Rapa Nui was not different among sites but was significantly higher at greater depths. Generally, the abundance of herbivorous fishes such as nānue is highest in shallow water and declines progressively as depth increases

(Brokovich et al., 2008; Friedlander et al., 2010). This pattern is correlated with the vertical distribution of algae, which is normally more abundant in shallow water and declines gradually with depth because of the decrease in light penetration (Hay, 1981). Thus, this inverse vertical pattern of distribution is not optimal for herbivore feeding, which suggests a possible negative effect of fishing on nānue local populations. Furthermore, the body

121 length of nānue was significantly larger (older and more experienced fish) at deeper depths, which also suggests a refuge from fishing.

Kyphosus sandwicensis is one of the most important recreational and commercially

(mostly for local consumption) coastal fish species for the Rapanui and has notable cultural significance. This species has seven secondary names based on size (e.g., “nānue pua” and

“nānue kekeho” for the smallest and largest respectively) and five secondary names based on color pattern (e.g., “nānue para” referring to a yellow color pattern, “nānue motea” to an albino color pattern, and “nānue aku aku” to a yellow-black spotted color pattern, among others) (Randall and Cea, 2011; Friedlander et al., 2018). This detailed naming is associated with various life history phases, which connotes a rich understanding of the ecology of the species (Friedlander et al., 2018). For example, nānue para, which is rarely seen at Rapa

Nui, is one of the most prized targets for spearfishers, as it is described by the Rapanui as the fish that leads the others in the nānue schools. Therefore, spearfishers firstly spear the nānue para to disorientate the school, and then continue catching the remaining fish. During this study, only 2 nānue para were studied for FID (one at la Pirámide and one at Poike), none of them allowed divers to get closer than ~ 6 m. Further research on this topic is necessary to test this local belief, which would strongly contribute to management strategies based on traditional ecological knowledge seeking the protection of local nānue populations from spearfishing.

In comparison with other fishing techniques, little is known about early spearfishing activities at Rapa Nui. Ayres (1980) described relics of small multiple barbed spears or sticks, called “ruruki”, which were probably used for coastal fishing. Nowadays, islanders noted the arrival of modern spearfishing guns in the 1980s with international commercial

122 flights arriving from Tahiti (Aburto, 2018). Spearfishing is becoming increasingly popular among islanders (native and immigrants) mainly for local consumption and recreational purposes, with little commercial effort at present. As with other artisanal fishing techniques at Rapa Nui (e.g., handline, gillnets), there are no regulations for spearfishing; thus, the expansion of this activity poses a serious threat to coastal fish populations, which are already in low abundances (Friedlander et al., 2013).

Spearfishing typically targets large animals with long life spans, slow growth, late maturation, and highly territorial behavior (Fisch et al., 2013; Giglio et al., 2017). Barneche and colleges (2018) described the hyperallometric relation between fish body length and the reproductive energy output, showing that larger fishes produce disproportionately more eggs than smaller fishes, thus the high selectivity of spearfishing focusing on large individuals may strongly affect reproductive success of local fish populations, and consequently, the functional role that these fishes have upon the entire ecosystem

(Sbragaglia et al., 2018; Skinner et al., 2019). These ecological consequences can be accentuated in highly overfished places, risking the sustainability of artisanal local fisheries and the resilience of the reef ecosystem.

Currently, overfishing is a persistent problem at Rapa Nui and the islanders are aware of it, describing a continual reduction of marine resources over the past 30 years

(Zylich et al., 2014; Aburto et al., 2017). Friedlander et al. (2013) highlighted the low fish biomass and the almost complete absence of top predators in Rapa Nui, likely because of overfishing, which is consistent with the observations by Petit et al. (unpubl. data) seven years later, and consistent with the description of the nānue behavior, biomass, and population size structure shown in this study.

123

Despite the establishment of the Rapa Nui MUMPA, which does not restrict artisanal fishing, the development of effective management strategies is urgently needed to protect the nearshore fish stocks and the fundamental role they exert upon the coastal benthic communities at Rapa Nui.

4.6. MANAGEMENT RECOMMENDATIONS

In 2018, the Chilean government and the Rapa Nui people collectively established the largest MPA in the South Pacific Ocean (Rapa Nui MUMPA). However, no management strategies have been implemented so far to conserve fish biodiversity and ecosystem functions. Therefore, based on our findings we recommend the following management strategies to be implemented:

i) The establishment of no-take zones at the Pirámide and Motu Nui to help

recover fish populations, especially to ensure the reproductive contribution of

larger individuals. Science suggests that protection of at least 30% of

representative areas is needed to conserve fish populations and ecosystem

function, particularly in overfished locations (Zhao et al., 2020).

ii) The establishment of minimum and maximum size limits for K. sandwicensis.

Twenty cm is the size at first sexual maturity for K. sandwicensis (Acuña et al.,

2018). More research is needed to assess the size with greater egg production in

K. sandwicensis, to establish a maximum catch size limit in addition to a

mininum.

124

iii) Create a regulatory frame to obtain information on coastal fish catch (e.g.,

location, species, reproductive status, number and size of individual fishes).

iv) Create a legal regulatory frame to limit the number of people allowed to

spearfish around the island and establish restrictions on the type of gear used

during the activity (i.e. the use of SCUBA tanks).

The degradation of nearshore fish at Rapa Nui is detrimental to the livelihoods of the

Rapanui people. The ocean is one of the main sources of subsistence and have tremendous cultural importance to the Rapanui. Historically in the Pacific Islands, resources management has been conducted by local users who often have have a profound knowledge of local resources (Friedlander et al., 2018; Friedlander and Gaymer, 2020). Thus, the inclusion of traditional ecological knowledge, combined with scientific knowledge is fundamental to the successful management of coastal reef communities at Rapa Nui.

4.7. ACKNOWLEDGEMENTS

We would like to thank C. González, N. Morales, C. Rua, M. Mieres, and ORCA diving center for their help in different steps of this study. To Lonto Icka and Christin Rapu that help to improve this manuscript providing their useful traditional ecological knowledge.

The Comisión Nacional de Investigación Científica y Tecnológica (CONICYT) grant N°

21170169 supported the data gathering and writing work of IPV. This study was financed by the Chilean Millennium Initiative, ESMOI.

125

Chapter 5

General conclusions

Photo: Camila González

126

CHAPTER 5

General conclusions

This study used different experimental and observational approaches to understand how fishing is affecting coastal ecological mechanisms at Rapa Nui. In chapter 2, the use of exclusion experiments demonstrated the ecological role of fishes on algal successional patterns and control of a possible invasive algae on the coral reefs at Rapa Nui and highlights the threat these reefs are facing if fishing pressure on coastal herbivores and predators does not decrease. In chapter 3, the mirror experiment showed a more intense territoriality behavior of a bottom-dwelling fish at Rapa Nui compared to MMHMP, evidencing a possible indirect effect of the reduced abundance of top predators and the successive prey release. These observations are consistent with the positive relationship between the number of the observed territorial attacks by damselfish against fishes and the abundance of direct competitors. In chapter 4 we showed that the overall FID of Kyphosus sandwicensis at MMHMP was significantly shorter compared the shallow depths at Rapa Nui, but not different from that at greater depth at Rapa Nui. Furthermore, the biomass and body length of the studied fishes were higher at deeper depths related to shallower depths. The later finding suggests that fishing is affecting fish anti-predator behavior at depths frequented by spearfishes and indicated that greater depths are a natural refuge from fishing at Rapa Nui.

Resource overexploitation is not new at Rapa Nui. Ecological and social collapse in the past triggered by the complete deforestation of the island has been well documented

(Diamond, 2005; Hunt and Lipo, 2006; Jarman et al., 2017; Lima, 2020). The current overfishing of marine resources is a substantial problem noticed by the Rapanui community and scientists. During the last 20 years, several investigations and traditional ecological

127 knowledge (TEK) have described the decline in coastal marine diversity in a wide variety of taxa such as the snail “pure” (Cipraea caputdraconis), the highly valued endemic lobster

“ura” (Panulirus pascuensis), the seabird “tavake”(Phaethon lepturus ), the algae “auke”

(Dyctiopteris australis), as well as coastal fishes such as the Galapagos shark “māngo”

(Carcharhinus galapagensis), the jacks “toremo” (Seriola lalandi), “ruhi” (Caranx lugubris) and po‘opo‘o (Pseudocaranx cheilio), the wrasses “mārari” (Anampses caeruleopunctatus) and “ra‘emea” (Thallasoma purpureum), the seabass kōpuku

(Acanthistius fuscus), the rudderfish “nānue” (Kyphosus sandwicensis), the virtually absent nibbler “māhaki” (Girella nebulosa), and the parrotfish “‘uhuhanga” (Leptoscarus vaigiensis), among others (Aires, 1980; Randall and Cea, 2011; Friedlander et al., 2013;

Gaymer et al., 2013; Aburto et al., 2016; Acuña et al., 2018).

In the past, fishes were reported to account for half of the protein consumed by the

Rapanui people and were in such abundance that “fishes could be caught with bare hands, holding them between your legs” (Wilhelm and Hulot, 1950; Jarman et al., 2017). In contrast, our surveys revealed low biomass in all experimental sites at Rapa Nui and low trophic level fishes as the most abundant component of the coastal fish assemblage, which coincides with the results evidenced by Friedlander et al. (2013), suggesting that no improvement has occurred since 2011, when the latter authors did their surveys. To confront this problem and to conserve the high endemism described for the island (~ 40% of the coastal fish assemblage, see Friedlander et al., (2013)), two Large-Scale Marine Protected

Areas (LSMPA) were created in the Easter Island Ecoregion: the “Motu Motiro Hiva

Marine Park” (MMHMP) around Salas & Gómez Island and the “Rapa Nui Multiple Uses

Marine Protected Area” (RNMUMPA) at Rapa Nui. Fishing is an important economic and

128 cultural activity in Rapa Nui, which contributes greatly to the local food supply (Aburto et al., 2016); consequently, the establishment of these LSMPAs generated profound conflicts within the Rapanui community and with the Chilean government (Aburto et al., 2020), resulting in little progress on management plans 10 years after the declaration of the

MMHMP and 3 years since RNMUMPA was declared (Petit et al. 2018).

Marine Protected Areas (MPAs) are one of the most common tools to protect species diversity and the ecosystem services supplied by the environment (Mellin et al., 2016;

Roberts et al., 2017). Recent investigations have demonstrated the positive effects that no- take MPAs have on recovering overexploited fish populations, conserving high biomass of fishes within their borders (Berneche et al., 2018; Graham et al., 2020). Therefore, MPAs not only effectively protect biodiversity but can also sustain fisheries in the long term when adequate management strategies are implemented. The absence or deficiency of management plans is currently one of the major impedements to effective MPAs worldwide and in Chile (Bonhan et al., 2008; Petit et al., 2018). Thus, developing specific management strategies for coastal fisheries in Rapa Nui such as 1) establishment of no-take areas in at least 30% of relevant ecosystems, such as areas with higher fish biomass and lower influence of fishing (e.g., Hanga Oteo, La Pirámide and Motu Nui in Rapa Nui); 2) banning fishing activities on fishes during their reproductive season; 3) establishment of minimum and maximum fish body length limits for extractive purposes; and 4) the creation of a regulatory frame for artisanal, sport and recreational fishing. All these strategies are relevant for recovering the nearshore fish stocks and to ensure the fundamental ecological role they play in the coastal benthic communities at Rapa Nui.

129

To complement the recommendations emerged from this thesis, further research is necessary on: 1) the reproductive biology of prized and ecologically relevant species (e.g.,

Acanturus leucopareius, Kyphosus sandwicensis, Pseudocaranx cheilio, Caranx lugubris,

Carcharhinus galapagensis, among others) due to the lack of information on their reproductive cycles at Rapa Nui; 2) fishes home ranges, specifically the vertical and horizontal movements across the different coasts of the island, which is crucial for future zonation of the RNMUMPA; 3) increase the knowledge related to the coastal artisanal and recreational landings to obtain a better understanding of actual fishing pressure, and how traditional/cultural activities are affecting coastal fish conservation. All the topics mentioned above would strongly contribute to a better understanding of the ecology of coastal fishes in the Easter Island Ecoregion.

The degradation of coastal fish and benthic communities at Rapa Nui would be detrimental to the local community, owing to the tremendous socio-cultural importance of a healthy ocean to Rapa Nui society and the local economy. Involving local communities in scientific research increases the acceptance of scientific knowledge into local populations and contextualizes scientific work with traditional ecological knowledge (Fisher, 2000;

Friedlander et al., 2018; Friedlander and Gaymer, 2020; Petit et al., 2020). The continued collaborative work among islanders, scientist, and the government will strongly contribute to the urgent need of the implementation of effective management strategies for the conservation of this unique Pacific island and the wellbeing of its people.

130

6. REFERENCES

Abrey, C. 2005. The effect of community on the territorial behavior of the three spot

damselfish. Environmental Biology of Fishes 73:163-170.

Aburto, J., Gaymer, C., Haoa, S. and González, L. 2015. Management of marine resources

through a local governance perspective: Re-implementation of traditions for marine

resource recovery on Easter Island. Ocean & Coastal Management 116: 108-115.

Aburto, J., Gaymer, C. and Cundill, G. 2016. Towards local governance of marine

resources and ecosystems on Easter Island. Aquatic Conservation: Marine and

Freshwater Ecosystems 30: 1765-1769.

Aburto, J. 2018. Informe final proyecto Post-doc Nº3160195.

Aburto, J., Gaymer, C. and Govan, H. 2020. A large-scale marine protected area for the sea

of Rapa Nui: From ocean grabbing to legitimacy. Ocean and Coastal Management

198: 2-13.

Acuña, E., Gaymer, C., Hinojosa, I., Aburto, J., Cortés, A., Sfeir, R., Petit, I. and Véliz, C.

2018. Estudio Biológico-Pesquero y Evaluación del Estado de Situación de Las

Pesquerías Costeras de Importancia Para la Isla de Pascua. FIPA Nº 2016-35.

Advani, S., Rix, L., Aherne, D., Alwany, M. and Bailey, D. 2015. Distance from a fishing

community explains fish abundance in a No-Take zone with weak compliance. PloS

ONE 10(5): 1-17.

131

Águila, B., Gaymer, C. and Aburto, J. 2020. Caracterización de la pesca de orilla en Rapa

Nui en función de las condiciones climáticas. Marine Biologist honor thesis.

Universidad Católica del Norte. 43 pp.

Anchieta, J., Blumstein, D., Giglio, V., Barros, F. and Quimbayo, P. 2019. Reef fish

antipredator behavior in remote islands does not reflect patterns seen in coastal

areas. Ethology Ecology & Evolution 31(6): 557-567.

Arias-González, J., Fung, T., Seymour, R., Garza-Pérez, J., Acosta-González, G., Bozec,

Y. and Johnson, C. 2017. A coral-algal phase shift in Mesoamerica not driven by

changes in herbivorous fish abundance. PloS ONE 12(4): 1-17.

Ayres, W. 1981. Easter Island Fishing. Asian Perspectives 22(1): 61-92.

Barneche, D., Robertson, R., White, C. and Marshall, D. 2018. Fish reproductive-energy

output increases disproportionately with body size. Science 360: 642-645.

Bates, D., Maechler, M., Bolker, B., Walker, S. 2015. Fitting Linear Mixed-Effects Models

Using lme4. Journal of Statistical Software 67(1): 1-48.

Begon, M., Townsend, C. and Harper, J. 1986. Ecology: From Individuals to Ecosystems.

4th ed. Wiley Blackwell. 750 pp.

Bertness, M. 1989. Intraspecific competition and facilitation in a Northern acorn barnacle

populaton. Ecology 70(1): 257-268.

Blumstein, D. 2005. The multipredator hypothesis and the evolutionary persistence of

antipredator behavior. Ethology 112: 209-217.

132

Bonham, A., Sacayon, E., Tzi, E. 2008. Protecting imperiled “paper parks”: potential

lessons from the Sierra Chinajá, Guatemala. Biodiversity and Conservation

17(7): 1581–93.

Brokovich, E., Einbinder, S., Shashar, N., Kiflawi1, M. and Kark, S. 2008. Descending to

the Twilight-zone: changes in coral reef fish assemblages along a depth gradient down

to 65 m. Marine Ecology Progress Series 371: 253-262.

Brown, J., Laundré, W. and Gurung, M. 1999. The ecology of fear: optimal foraging, game

theory, and trophic interactions. Journal of mammalogy 80(2): 385-399.

Burkepile, D. and Hay, M. 2008. Herbivore species richness and feeding complementarity

affect community structure and function on a coral reef. Proceedings of the National

Academy of Sciences 105(42): 16201–16206.

Burkepile, D. and Hay, M. 2010. Impact of herbivore indentity on algal succession and

coral growth on a Caribbean reef. PloS ONE 5(1): e8963.

Canan, B., Pessoa, E., Volpato, G., Araújo, A. and Chelleppa, S. 2011. Feeding and

reproductive dynamics of the damselfish, Stegastes focus in the coastal reefs of

northeastern Brazil. Animal Biology Journal 2(3): 113:126.

Ceccarelli, D., Jones, G. and McCook, J. 2011. Interactions between herbivorous fish guilds

and their influence on algal succession on a coastal coral reef. Journal of Experimental

Marine Biology and Ecology 399(1): 60-67.

133

Cech, L. 2016. Nesting behavior of Acapulco damselfish (Stegaste acapulcoensis): pairs

defend nest more vigorously than solitary males. Departament of Molecular and

Cellular Biology, University of California. 12 pp.

Chase, J., Abrams, P., Grover, J., Diehl, S., Chesson, P., Holt, R., Richards, S., Nisbet, R.

and Case, T. 2002. The interaction between predation and competition: a review and

synthesis. Ecology Letters 5(2): 302-315.

Cheal, A., Emslie, M., MacNeil, A., Miller, I. and Sweatman, H. 2013. Spatial variation in

the functional characteristics of herbivorous fish communities and the resilience of

coral reefs. Ecological Applications 23(1): 174-188.

Clements, F. 1916. Plant succession: an analysis of the development of vegetation. Carnegie

Institute of Washington 242. Washington, DC.

Cody, L., MacArthur, R. and Diamond, M. 1975. Ecology and Evolution of Communities.

Harvard University Press, Cambridge, Massachusetts. 507 pp.

Connell, J. and Slatyer, R. 1976. Mechanisms of succession in natural communities and

their role in community stability and organization. The American Naturalist

111(982): 1119-1144.

Connell, J. 1983. On the prevalence and relative importance of interspecific competition:

evidence from field experiments. The American Naturalist 122(5): 662: 696.

Collias, N. 1944. Behavior among vertebrate animals. University of Chicago Press 17: 83-

123.

134

Davis, K., Carlson, P., Bradley, D., Warner, R. and Caselle, J. 2017. Predation risk

influences feeding rates but competition structures space use for a common Pacific

parrotfish. Oecologia 184:139-149.

Del Río, L., Vidal, J., Betancor, S. and Tuya, F. 2016. Differences in herbivory intensity

between the seagrass Cymodocea nodosa and the green alga Caulerpa prolifera

inhabiting the same habitat. Aquatic Botany 128: 48-57.

DeMartini, E., Friedlander, A., Sandin, S. and Sala, E. 2008. Differences in fish-

assemblages structure between fished and unfished atolls in the northern Line

Islands, central Pacific. Marine Ecology Progress Series 365: 199-215.

Diamond, J. 2005. Collapse, How Societies Choose To Fail or Succeed. Viking press. 571

Pp.

DiSalvo, L., Randall, J., and Cea, A. 1988. Ecological reconnaissance of the Easter Island

sublittoral marine environment. National Geographic Research 4(4): 451–473.

DiSalvo, L., Randall, J., and Cea, A. 2007. Stomach contents and feeding observations of

some Easter Island fishes. Atoll Research Bulletin 548: 1-22.

Douglas, B., Martin, M., Bolker, B. and Walker, S. 2015. Fitting Linear Mixed-Effects

Models Using lme4. Journal of Statistical Software, 67(1): 1- 48.

Easton, E., Gaymer, C., Friedlander, A. and Herlan, J. 2018. Effect of herbivores, wave

exposure and depth on benthic coral communities of the Easter Island ecoregion.

Marine and Freshwater Research 69(6): 997-1006.

135

Edwards, C., Friedlander, A., Green, A. and Hardt, M. 2013. Global assessment of the status

of coral reef herbivorous fishes: evidence for fishing effects. Proceedings of the Royal

Society 281: 20131835.

Estes, J., Terborgh, J., Brashares, J., Power, M., Berger, J., Bond, W., Carpenter, S.,

Essington, T., Holt, R., Jackson, J. and Marquis, R., 2011. Trophic downgrading of

planet Earth. science, 333(6040): 301-306.

Feary, D., Cinner, J., Graham, N. and Januchowski-Hartley, F. 2010. Effects of customary

marine closures on fish behavior, spear-fishing success, and underwater visual

surveys. Conservation Biology 25(2): 341-349.

Fishelson, D., Popper, D. and Avidor, A. 1974. Biosociology and ecology of pomacentrid

fishes around the Sinai Peninsula (northern Red Sea). Journal of Fish Biology 6:

119-133.

Fisher, F. 2000. Citizens, Experts, and the Environment: The Politics of Local Knowledge.

Durham, NC: Duke University Press.

Fisher, L. and Norris, M. 1960. Bathymetry and geology of Salas y Gómez southeast

Pacific. Geological Society of America Bulletin 71: 497–502.

Fong, P., and Paul, J. 2011. Coral reef algae. In: An Ecosystem in Transition. (Eds.

Dubinsky and N. Stambler.) pp. 241-272. (Springer: Dordrecht, Netherlands.)

Fox, R. and Bellwood, D. 2007. Quantifying herbivory across a coral reef depth gradient.

Marine Ecology Progress Series 338: 49-59.

136

Friedlander, A. and Parrish, J. 1998. Habitat characteristics affecting fish assemblages on a

Hawaiian Coral Reef. Journal of Experimental Marine Biology and Ecology 224: 1-

30.

Friedlander, A. and DeMartini, E. 2002. Contrasts in density, size, and biomass of reef

fishes between the northwestern and the main Hawaiian Islands: The effects of fishing

down apex predators. Marine Ecology Progress Series 230: 253-264.

Friedlander, A. and Brown, E. 2005. Hanalei Bay, Kaua`I marine benthic communities

since 1992: spatial and temporal trends in a dynamic Hawaiian coral reef ecosystem.

Hawaii Cooperative Studies Unit Technical Report HCSU-003. University of

Hawaii at Hilo. 32 pp.

Friedlander, A., Sandin, S., DeMartini, E. And Sala, E. 2010. Spatial patterns of the

structure of reef fish assemblages at a pristine atoll in the Central Pacific. Marine

Ecology Progress Series 410: 219-231.

Friedlander, A., Ballesteros, E., Beets, J., Berkenpas, E., Gaymer, C., Gorny, M. and Sala,

E. 2013. Effects of isolation and fishing on the marine ecosystems of Easter Island

and Salas y Gómez, Chile. Aquatic Conservation: Marine and Freshwater Ecosystems

23: 515–531.

Friedlander, A. 2018. Marine conservation in Oceania: Past, present, and future. Marine

Pollution Bulletin, 135: 139-149.

137

Friedlander, A. and Gaymer, C. 2020. Progress, opportunities and challenges for marine

conservation in the Pacific Islands. Aquatic Conservation: Marine Fresh Water

Ecosystems 1-11.

Frisch, A., Cole, A., Hobbs, J., Rizzari, J. and Munkres, K. 2012. Effects of spearfishing on

reef fish populations in a multi-use conservation area. PLoS ONE 7(12): e51938.

Froese, R. and Pauly, D. 2011. FishBase. World Wide Web electronic publication,

www.fishbase.org.

Gálvez-Larach, M. 2009. Seamounts of Nazca and Salas y Gómez: a review for

management and conservation purposes. Latin American Journal of Aquatic Research

37(3), 479–500.

Gaymer, C. and Himmelman, J. 2008. A keystone predatory sea star in the intertidal zone

is controlled by a higher-order predatory sea star in the subtidal zone. Marine Ecology

Progress Series 370: 143-153.

Gaymer, C., Carcamo, F., Friedlander, A., Palma, A., Bodini, A. et al. 2011.

Implementación de una Reserva Marina en la bahía de Hanga Roa: estudio de línea

de base. Facultad de Ciencias del Mar, Universidad Católica del Norte, Coquimbo.

144 pp.

Gaymer, C., Aburto, J., Acuña, E., Bodini, A., Carcamo, F., Tapia, C. and Stotz, W. 2013.

Base de conocimiento y construcción de capacidades para el uso sustentable de los

ecosistemas y recursos marinos de la ecorregión de Isla de Pascua. Informe Final

Proyecto SUBPESCA Licitación (4728-33).

138

Gehrt, S. and Prange, Z. 2006. Interference competition between coyotes and raccoons: a

test of the mesopredator release hypothesis. Behavioral Ecology 204-215.

Giglio, V., Bender, M. Zapelini, C. and Ferreira, C. 2017. The end of the line? Rapid

depletion of a large-sized grouper through spearfishing in a subtropical marginal

reef. Perspectives in Ecology and Conservation 15: 115-118.

Godoy, N., Gelcich, E., Vázquez, J. and Castilla, J. 2010. Spearfishing to depletion:

evidence from temperate reef fishes in Chile. Ecological Applications 20(6):1504-

1511.

Gotanda, K., Turgeon, K. and Kramer, D. 2009. Body size and reserve protection affect

flight initiation distance in parrotfishes. Behavioral Ecology and Sociobiology 63:

1563-1572.

Graham, N., Robinson, J., Smith, S., Govinden, R., Gendron, G. and Wilson, S. 2020.

Changing role of coral reef marine reserves in a warming climate. Nature

communications 11(1) : 1-8.

Haley, M. and Muller, C. 2002. Territorial behavior of beaugregory damselfish (Stegastes

leucostictus) in response to egg predators. Journal of Marine Biology and Ecology

273: 151-159.

Hamb, A. 2011. Defense of multi-functional territory against interspecific intruders by the

damselfish Stegastes nigricans (Pisces, Pomacentridae). UC Berkeley: UCB

Moorea Class: Biology and Geomorphology of Tropical Islands.

139

Hay, M. 1981. Herbivory, algal distribution, and the maintenance of between-habitat

diversity on a tropical fringing reef. The American Naturalist, 118(4): 520-540.

Heil, C., Chaston, K., Jones A., Bird P., Longstaff B., Costanzo S. and Dennison. 2004.

Benthic microalgae in coral reef sediments of the southern Great Barrier Reef,

Australia. Coral Reefs 23: 336-343.

Hess, S., Fischer, S. and Taborsky, B. 2016. Territorial aggression reduces vigilance but

increases aggression towards predators in a cooperatively breeding fish. Animal

Behavior 113: 229-235.

Hixon, M. and Brostoff, N. 1983. Damselfish as keystone species in reverse: intermediate

disturbance and diversity of reef algae. Science 220:511–513.

Hixon, M. and Brostoff, N. 1996. Succession and herbivory: effects of differential fish

grazing on Hawaiian coral-reef algae. Ecological Monograph 66:67–90.

Hixon, M. 1998. Effects of reef fishes on corals and algae. 231-248. Birkeland C. In: Life

and Death of Coral Reefs. Chapman and Hall. USA. 536 pp.

Hixon, M. 2015. Reef fishes, seaweeds, and coral: A complex triangle. 195-216. Birkeland

C. In: Coral Reed in the Anthropocene. Springer. USA. 271 pp.

Horne, E. and Itzkowitz, M. 1995. Behavior of the female beaugregory damselfish

(Stegastes leucostictus). Journal of Fish Biology 46: 457-461.

Hubbard, D. and García, M. 2003. The corals and coral reefs of Easter Island – A

preliminary look. 53 – 77. In: Easter Island, Scientific Exploration into the World´s

Environmental Problems in Microcosm. 175 pp.

140

Hughes, T., Szmant A., Steneck, R., Carpenter, R. and Miller, S. 1999. Algal blooms on

coral reefs: What are the causes? Limnology and Oceanography 44:1583–1586.

Hunt, T. and Lippo, C. 2006. Late colonization of Easter Island. Science 311: 1603-1606.

Huntingford, F. 1982. Do inter- and intraspecific aggression vary in relation to predation

pressure in stricklebacks? Animal Behavior 30:909-916.

Jarman, C., Larsen, T., Hunt, T., Lipo, C., Solsvik, R., Wallsgrove, N., Ka’apu-Lyons, C.,

Close, H. and Popp, B. 2017. Diet of the prehistoric population of Rapa Nui (Easter

Island, Chile) shows environmental adaptation and resilience. Physical Anthropology

1-19.

Januchowski-Hartley, A., Graham, N., Feary, D., Morove, T. and Cinner, J. 2011. Fear of

fishers: human predation explains behavioral changes in coral reef fishes. PLoS ONE

6(8): e22761.

Januchowski-Hartley, A., Nash, K. and Lawton, R. 2012. Influence of spearguns, dive gear

and observers on estimating fish flight initiation distance on coral reefs. Marine

Ecology Progress Series 469: 113–119.

Jompa, J. and McCook, L. 2002. Effects of competition and herbivory on interactions

between a hard coral and a brown alga. Journal of Experimental Marine Biology and

Ecology 271: 25-39.

Karino, K. and Nakazono, A. 1993. Reproductive behavior of the territorial herbivore

Stegastes nigricans (pisces: Pomacentridae) in relation to colony formation. Journal

of Ethology 11: 99-110.

141

Kulbicki, M. 1998. How the acquired behavior of commercial reef fishes may influence the

results obtained from visual censuses. Journal of Experimental Marine Biology and

Ecology 222: 11-30.

Lee, G. 2004. Rapa Nui´s sea creatures. Rapa Nui Journal: Journal of the Easter Island

Foundation 18(12): 31-38.

Lewis, S. and Wainwright, P. 1985. Herbivore abundance and grazing intensity on a

Caribbean Coral Reef. Journal of Experimental Marine Biology and Ecology 87: 215-

228.

Lima, M. and Dill, M. 1990. Behavioral decisions made under the risk of predation: a

review and prospectus. Canadian Journal of Zoology. 68: 619–640.

Lima, M. 1998. Nonlethal effects in the ecology and predator-prey interactions. Bioscience.

48: 25–34.

Lima, M., Gayo, E., Latorre, C., Santoro, C., Estay, A., Cañellas-Bolta, N., Margalef, O.,

Giralt, S., Sáez, A., Pla-Rabes, S. and Stenseth, N. 2020. Ecology of the collapse of

Rapa Nui society. Proceedings B 287: 20200662.

Lindfield, S., McIlwain, J. and Harvey, E. 2014. Depth refuge and the impacts of SCUBA

spearfishing on coral reef fishes. PLoS ONE 9(3): e92628.

Lindfield, S., Harvey, E., Halford, A. and McIlwain, J. 2015. Mesophotic depths as refuge

areas for fishery-targeted species on coral reefs. Coral Reefs 35(1): 125-137.

Little, K., Draud, M. and Itzkowitz. 2013. aggression in two highly similar Stegastes

damselfish, Ethology Ecology & Evolution 25: 227-242.

142

Lloret, J., Zaragoza., N., Caballero, D., Font, T., Casadevall, M. and Riera, V. 2008.

Spearfishing pressure on fish communities in rocky coastal habitats in a

Mediterranean marine protected area. Fisheries Research 94:84-91.

Lubchenco, J. 1978. Plant species diversity in a marine intertidal community: importance

of herbivore food preference and algal competitive abilities. The American

Naturalist 11(983): 23-39.

Luypaert, T., Hagan, J., McCarthy., M. and Poti, M. 2020. Status of marine biodiversity in

the Anthropocene. In: Youmares 9- The Oceans: Our Research, Our Future. 370 pp.

Madin, E., Gaines, S. and Warner, R. 2010. Field evidence for pervasive indirect effects of

fishing on prey foraging behavior. Ecology 91(12): 3563-3571.

Marshell, A. and Mumby, P. 2015. The role of surgeonfish (Acanthuridae) in maintaining

algal turf biomass on coral reefs. Journal of Experimental Marine Biology and

Ecology 473: 152-160.

McCook, L. 2001. Competition between corals and algal turfs along a gradient of terrestrial

influence in the nearshore central Great Barrier Reef. Coral Reefs 19: 419-425.

Mellin, C., MacNeil, A., Cheal, A., Emslie, M. Caley, J. 2016. Marine protected areas

increase resilience among coral reef communities. Ecology Letters 19(6): 629-

637.

Morales, N., Easton, E., Friedlander, A., Harvey, E., Garcia, R. and Gaymer, F. 2019.

Spatial and seasonal differences in the top predators of Easter Island: Essential data

143

for implementing the new Rapa Nui multiple-uses marine protected area. Aquatic

Conservation Marine and Freshwater Ecosystems 29: 118-129.

Morin, J. 1986. Interactions between intraspecific competition and predation in an

amphibian predator-prey system. Ecology 67(3): 713-720.

Morrison, D. 1986. Algal-herbivore interactions on a Jamaican coral reef. Doctoral

Dissertation. University of Georgia, USA.

Moyle, B. and Cech, J. 2004. Fishes: An Introduction to Ichthyology. 5th ed. Pearson,

Benjamin Cummings. San Francisco, USA. 726 pp.

Mumby, P. 2006. Fishing, trophic cascades, and the process of grazing on coral reefs.

Science 311: 98-101.

Mumby, P., Hastings, A. and Edwards, H. 2007. Thresholds and the resilience of Caribbean

coral reefs. Nature Letters 450: 98-101.

Mumby, P. 2016. Stratifying herbivore fisheries by habitat to avoid ecosystem overfishing

of coral reefs. Fish and Fisheries. 17(1): 266-278.

Newman, M., Paredes, G., Sala, E. and Jackson, J. Structure of Caribbean coral reef

communities across a large gradient of fish biomass. Ecology Letters 9:1216-1227.

Oksanen, J., Blanchet, G., Friendly, M., Kindt, R., Legendre, P., McGlinn, D., Minchin, P.,

O’Hara, R., Simpson, G., Solymos, P., Stevens, H., Szoecs, E. and Wagner, H. 2019.

vegan: Community Ecology Package. R package version 2.5-6. https://CRAN.R-

project.org/package=vegan

144

Oliveira, R., Pereira, C., Pimentel, A. and Schlindwein, C. 2016. The consequences of

predation risk on the male territorial behavior in a solitary bee. Ethology 122:1-8.

Paine, R. 1966. Food web complexity and species diversity. American Naturalist 100:65-

75.

Petit, I., Campoy A., Hevia, M., Gaymer, C. and Squeo, F. 2018. Protected areas in Chile,

are we managing them? Revista Chilena de Historia Natural 91(1): 1-8.

Petit, I., González, C., Gusmao, J., Álvarez-Varas, R. and Hinojosa, A. 2020. Resting

dynamics and diel activity of the green turtle (Chelonia mydas) in Rapa Nui,

Chile. Chelonian Conservation and Biology 19(1): 124:132.

Petit, I., Gaymer, C., Friedlander, A. and Gusmao, J. (in preparation). Human at the top of

the food web: are coastal benthic communities in Rapa Nui affected by fishing?

Power, E., Stewart, A. and Matthews, W. 1988. Grazer control of algae in an Ozark

mountain stream: effects of short-term exclusion. Ecology 69(6): 1894-1898.

Poepoe, K., Bartram, P. and Friedlander, A. 2007. The use of traditional Hawaiian

knowledge in the contemporary management of marine resources. Pages 117-141 in:

Fishers' knowledge in fisheries science and management (N. Haggan, B. Neis, and

I.Baird, eds.). UNESCO, Paris.

R Core Team. 2014. R: A language and environment for statistical computing. R

Foundation for Statistical Computing, Vienna, Austria.

Randall, J. and Cea, A. 2011. Shore Fishes of Easter Island. University of Hawaii Press,

Honolulu, USA. 154 pp.

145

Roberts, C., O’Leary, B., McCauley, D., Cury, F. Duarte, C., Lubchenco, J., Pauly, D.

Sáenz-Arroyo, A., Sumaila, U., Wilson, R., Worm, B., and Castilla, J. 2017.

Marine reserves can mitigate and promote adaptation to climate change.

Proceedings of the National Academy of Sciences 114(24): 6167-6175.

Sandin, S., Smith, J., DeMartini, E., Dinsdale, E., Donner, S., Friedlander, A., Kootchick,

T, Malay, M., Maragos, J., Obura, D., Pantos, O., Paulay, G., Richie, M., Rohwer, F.,

Schroeder, R., Walsh, S., Jackson, J., Knowlton, N. and Sala, E. 2008. Baselines and

degradation of coral reefs in the Northern line Islands. PloS ONE 3(2): 1-11.

Santelices, B. 1987. Flora marina bentónica de las islas oceánicas Chilenas. In: Islas

Oceánicas Chilenas: Conocimiento Científico y Necesidades de Investigaciones,

101-125 pp. Ed. Castilla, J. Ediciones Universidad Católica de Chile. 353 pp.

Santelices, B. and Abbott, A. 1987. Geographic and marine isolation: An assessment of the

marine algae of Easter Island. Pacific Science 41: 1-4.

Santelices, B. and Meneses, I. 2000. A reassessment of the phytogeographic

characterization of temperate Pacific South America. Revista Chilena de Historia

Natural 73: 605–614.

Santiañez, J., Macaya, E., Kyung, L., Cho, G., Boo, S. and Kogame, K. 2018. Taxonomic

reassessment of the Indo-Pacific Scytosiphonaceae (Phaeophyceae): Hydroclathrus

rapanuii sp. nov. and Chnoospora minima from Easter Island, with proposal of

Dactylosiphon gen. nov. and Pseudochnoospora gen. nov. Botanica Marina, 61(1):

47-64.

146

Sala, E. and Boudouresque, C. 1997. The role of fishes in the organization of a

Mediterranean sublittoral community. I: Algal communities. Journal of Experimental

Marine Biology and Ecology 212: 25-44.

Sbragaglia, V., Morroni, L., Bramanti, L., Weitzmann, B., Arlinghaus, R. and Azzurro, E.

2018. Spearfishing modulates flight initiation distance of fishes: the effects of

protection, individual size, and bearing a speargun. Journal of Marine Science 75(5):

1779-1789.

Schall, J. and Pianka, R. 1980. Evolution of escape behavior diversity. The American

Naturalist 115(4): 551-566.

Seghers, H. 1976. Schooling behavior in the guppy (Poecilia reticulata): an evolutionary

response to predation. Evolution 28: 486-489.

Silvano, R., Nora, V., Andreoli, T., Lopes, P. and Begossi, A. 2017. The “ghost of past

fishing”: small-scale fisheries and conservation of threatened groupers in subtropical

islands. Marine Policy 75:125 -132.

Skinner, C., Neman, S., Box, S., Narozanski, A. and Polunin, N. 2019. Chronic spearfishing

may indirectly affect reef heath through reductions in parrotfish bite rates. Journal

of Fish Biology 94(4): 585-594.

Stamoulis, K., Friedlander, A., Meyer, C., Fernandez-Silva, I. and Robert, T. 2017. Coral

reef grazer-benthos dynamics complicated by invasive algae in a small marine

reserve. Scientific Reports 7: 43819.

147

Stamoulis, K., Delevaux, J., Williams, I., Friedlander, A., Reichard, J. Kamikawa, K. and

Harvey, E. 2020. Incorporating reef fish avoidance behavior improves accuracy of

species distribution models. PeerJ 8: 2-21.

Steneck, R., David, R. and Hay, M. 2017. Herbivory in the Marine Realm. Current Biology

27(11): R484-R489.

Szmant, A. 2001. Introduction to the special issue of Coral Reefs on ‘‘Coral Reef Algal

Community Dynamics.’’ Why are coral reefs world-wide becoming overgrown by

algae? ‘Algae, algae everywhere, and nowhere a bite to eat!’ Coral Reefs 19:299–

302.

Terborgh, J. and Estes J. 2010. Trophic Cascades, Predators, Prey, and the Changing

Dynamics of Nature. Island press. Washington, USA. 464 pp.

Tran, D., Langel, K., Thomas, M. and Blumstein. 2016. Spearfishing-induced behavioral

changes of an unharvested species inside and outside a marine protected area.

Current Zoology 61(1): 39-44.

Underwood, A. 2009. Components of design in ecological field experiments. Annales

Zoologici Fennici 46: 93-111.

Uribe, R., Ortiz, M., Macaya, E. and Pacheco, A. 2015. Successional patterns of hard-

bottom macro benthic communities at kelp bed (Lessonia trabeculata) and barren

ground sublittoral systems. Journal of Experimental Marine Biology and Ecology

472: 180-188.

148

Urriago, J., Himmelman, J. and Gaymer, C. 2011. Responses of the black sea urchin

Tetrapygus niger to its sea-star predators Heliaster helianthus and Meyenaster

gelatinosus under field conditions. Journal of Experimental Marine Biology and

Ecology 399: 17-24.

Wang, Y., Naumann, U., Wright, T. and Warton, I. 2012. mvabund - an R package for model-based analysis of multivariate abundance data. Methods in Ecology and Evolution

3: 471–474.

Wernberg, T. and Connell, S. 2008. Physical disturbance and subtidal habitat structure on

open rocky coasts: effects of wave exposure, extent and intensity. Journal of Sea

Research 59: 237-248.

Westafall, P. and Young, S. 1993. Resampling-based Multiple Testing. John Wiley & Sons.

New York.

Wilhelm, O. and Hulot, A. 1954. Pesca y peces de la Isla de Pascua. In: Boletin de la

Sociedad de Biología de Concepción. Universidad de Concepción 139-152.

Williams, I., Walsh, W., Schroeder, R., Friedlander, A., Richards, B., and Stamoulis, K.

2008. Assessing the importance of fishing impacts on Hawaiian coral reef fish

assemblages along regional-scale human population gradients. Environmental

Conservation 35(3): 261-272.

Williams, J., Smith, E., Conklin, J., Gove, M., Sala, E. and Sandin, A. 2013. Benthic

communities at two remote Pacific coral reefs: effects of reef habitat, depth and wave

energy gradients on spatial patterns. PeerJ 1: e81.

149

Worm, B. and Paine, R. 2016. Humans as a hyperkeystone species. Trends in Ecology &

Evolution (31)8: 600-607.

Ydenberg, C. and Dill, M. 1986. The economics of fleeing from predators. Advances in the

Study of Behavior 16: 229−249.

Zhao, Q., Stephenson, F., Lundquist, C., Kaschner, K., Jayathilake, D. and Costello, M.

2020. Where Marine Protected Areas would best represent 30% of ocean biodiversity.

Biological Conservation 244: 108536.

Zylich, K., Harper, S., Licandeo, R., Vega, R., Zeller, D. and Pauly, D. 2014. Fishing in

Easter Island, a recent history (1950-2010). Latin American Journal of Aquatic

Research 42(4): 845-856.

150