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Evolutionary Island Biogeography: Origins and Maintenance of Fish Biodiversity in Marine Lakes

Periodic Reporting for period 1 - ADAPTIVEISLANDS (Evolutionary Island Biogeography: Origins and Maintenance of Fish Biodiversity in Marine Lakes)

Reporting period: 2022-10-01 to 2024-09-30

ADAPTIVEISLANDS: Evolutionary Island Biogeography: Origins and Maintenance of Fish Biodiversity in Marine Lakes
Why do some islands host unique species while others do not? How do species adapt to isolation over time? The ADAPTIVEISLANDS project explores these fundamental questions by testing Evolutionary Island Biogeography in a natural experiment: the marine lakes of Raja Ampat, Indonesia. These isolated pockets of seawater, connected to the ocean through cracks and tunnels, create a real-world laboratory for studying how species colonize, persist, and adapt in isolated environments.
ADAPTIVEISLANDS focuses on three key questions:
How does isolation shape biodiversity? We compiled a database of fish diversity in marine lakes to study how sea connectivity and species dispersal traits affect fish community diversity.
How does isolation impact colonization and extinction? We are working on reconstructing the historical colonization-extinction dynamics of two fish species, which differ in their ability to disperse, using sediment cores.
How does isolation drive adaptation? By studying fish populations in lakes with varying levels of connectivity (low, medium, high), we are exploring how species adapt to challenging environmental conditions, such as differences in salinity and temperature.
By integrating fieldwork, genetics, and ecological modeling, ADAPTIVEISLANDS provides new insights into the evolutionary and ecological processes shaping biodiversity in fragmented habitats. These findings will help inform marine conservation strategies, particularly in environments vulnerable to climate change and human impact. This research aims to bridge the gap between classical island biogeography and evolutionary processes, advancing our understanding of how colonization, extinction, and adaptation interact to drive biodiversity.
WP1 aimed to create a database of fish diversity in marine lakes and examine the drivers of diversity. To understand the drivers of diversity and community assembly, I first built a database of all species that could potentially live in those systems (D.1.1). This database consisted of all reef-associated fish species (~1,100 species) occurring in the Raja Ampat Region (sensu Allen & Adrim 2003). Information on species traits was gathered from the literature and online databases. Phylogenetic imputation was used to fill in missing data using the Fish Tree of Life phylogeny (Rabosky et al 2018).
In 2023, I carried out six weeks of fieldwork in Indonesia (D.1.2) together with Dr. Becking, one master's student (Francesco Pelizza), two PhD students (Stephanie Martinez and Mainah Folkers) and four Indonesian partners (Niken Oktaviandini, Dea Lestari, Beginer Subhan from Bogor University and Awaludinnoer Ahmad from the Nature Conservancy). We visited 11 marine lakes and I sampled the fish communities using 25m video transects (6-10 transects per lake) and 20 min standing camera videos.
The data from this project has been analyzed and is currently being prepared for publication (D1.3).

WP2 aimed to reconstruct the historic colonization-extinction dynamics in marine lakes of two fish species with different dispersal characteristics (i.e. different dispersal-related traits): the Puntang goby, Exyrias puntang, and the Half-barred cardinal, Fibramia thermalis. Together with two PhD students and one master's student, I have received training from the University of Amsterdam (Prof. William Gosling and Dr. Majoi de Novaes Nascimento) on sediment coring techniques, especially living stone coring (D4.4). I had several meetings with Bern and Basel University researchers (Moritz Muschick and Nare Ngoepe) on sediment core preparation and ancient DNA analyses (D4.3).
I did fieldwork on Kri Island in Raja Ampat and collected six sediment cores from two marine lakes (D2.1). We could sample only two lakes in a single region, primarily because this was the only area with cooling facilities (air conditioning) to preserve cores for DNA analysis. Additionally, while other marine lakes existed within the region, we could not access them due to the presence of saltwater crocodiles in these lakes, which have been in the sampling plan.

WP3 aimed to test how different levels of isolation (low, medium, and high) from the sea affect biological adaptation to marine lakes, using the Puntang goby and the Half-barred cardinal. Due to restrictions on fish collection in the marine lakes, we decided to limit our analyses to samples collected by the Becking lab in 2020. Therefore, only Puntang goby samples will be considered. DNA extractions from fin clip tissue are being conducted at the Naturalis Biodiversity Center by a master's student and a lab technician (D3.1). I hope they will be completed by the end of the year. As we deviated from the initial question, we also incorporated morphometric and isotope data from the same specimens to examine whether adaptation results in genetic, morphological, and ecological divergence. Morphometric data has already been measured by PhD student Stephanie Martinez, while isotope analyses are being conducted by the master's student. Unfortunately, we cannot differentiate between males and females, as only fin clips were collected.
1.2.1 Work Package 1 – Marine lakes’ biodiversity patterns
WP1 aimed to create a database of fish diversity in marine lakes and examine the drivers of diversity. To understand the drivers of diversity and community assembly, I first built a database of all species that could potentially live in those systems (D.1.1). This database consisted of all reef-associated fish species (~1,100 species) occurring in the Raja Ampat Region (sensu Allen & Adrim 2003). Information on species traits was gathered from the literature and online databases. Phylogenetic imputation was used to fill in missing data using the Fish Tree of Life phylogeny (Rabosky et al 2018).
In 2023, I carried out six weeks of fieldwork in Indonesia (D.1.2) together with Dr. Becking, one master's student (Francesco Pelizza), two PhD students (Stephanie Martinez and Mainah Folkers) and four Indonesian partners (Niken Oktaviandini, Dea Lestari, Beginer Subhan from Bogor University and Awaludinnoer Ahmad from the Nature Conservancy). We visited 11 marine lakes and I sampled the fish communities using 25m video transects (6-10 transects per lake) and 20 min standing camera videos.
The data from this project has been analyzed and is currently being prepared for publication (D1.3).

Transfer of knowledge: During this project, I supervised two PhD students and one master's student during fieldwork, and I supervised three master's students during their theses:
MSc Francesco Pelizza, thesis: understanding fish biodiversity in marine lakes
MSc student Noortje Barning, thesis: the effect of habitat condition on ecosystem functioning of coral reef fish communities in Raja Ampat, Indonesia
MSc student Maarten Hoepel, thesis: Determinants of tropical fish diversity in marine lakes: a case study in Island Biogeography theory in Raja Ampat, Indonesia
I have trained the master students on fish identification, data collection and analyses, fish sampling, statistical analyses and phylogenetic data imputation. I also trained a WUR colleague professor (Dr. Nagelkerke) on phylogenetic imputation techniques for imputing missing trait data.

We presented our work plan to the government authorities in Indonesia BRIN and Papua and Bogor University, together with a workshop for knowledge sharing (D.5.3). The results of this WP have been presented in several scientific conferences (D5.4) as described below.

State of the art: This study is the first attempt to describe marine lake fish communities and to investigate how biodiversity arises and thrives in these isolated ecosystems with sometimes extreme environments, which is relevant in a world where nature is becoming increasingly fragmented and warmer.
1.2.2 Work Package 2 – Historical ecological dynamics
WP2 aimed to reconstruct the historic colonization-extinction dynamics in marine lakes of two fish species with different dispersal characteristics (i.e. different dispersal-related traits): the Puntang goby, Exyrias puntang, and the Half-barred cardinal, Fibramia thermalis. Together with two PhD students and one master's student, I have received training from the University of Amsterdam (Prof. William Gosling and Dr. Majoi de Novaes Nascimento) on sediment coring techniques, especially living stone coring (D4.4). I had several meetings with Bern and Basel University researchers (Moritz Muschick and Nare Ngoepe) on sediment core preparation and ancient DNA analyses (D4.3).
I did fieldwork on Kri Island in Raja Ampat and collected six sediment cores from two marine lakes (D2.1). We could sample only two lakes in a single region, primarily because this was the only area with cooling facilities (air conditioning) to preserve cores for DNA analysis. Additionally, while other marine lakes existed within the region, we could not access them due to the presence of saltwater crocodiles in these lakes, which have been in the sampling plan.

Transfer of knowledge: During this project, I supervised one master's student during fieldwork on coring techniques. We presented our work plan to the government authorities in Indonesia BRIN and Papua and Bogor University, together with a knowledge-sharing workshop (D.5.3).

State of the art: The application of ancient DNA (aDNA) for community dynamics is still in the early stages, but it provides highly valuable insights. Unfortunately, logistical challenges in the field due to the presence of crocodiles prevented the collection of the planned number of sediment cores. Specifically, using aDNA to study biodiversity required the cores to be stored at low temperatures during sampling. Thus, we could only focus on a region in Raja Ampat with adequate air conditioning. In that region, we could only access two crocodile-safe lakes.
1.2.3 Work Package 3 – Local adaptation

WP3 aimed to test how different levels of isolation (low, medium, and high) from the sea affect biological adaptation to marine lakes, using the Puntang goby and the Half-barred cardinal. Due to restrictions on fish collection in the marine lakes, we decided to limit our analyses to samples collected by the Becking lab in 2020. Therefore, only Puntang goby samples will be considered. DNA extractions from fin clip tissue are being conducted at the Naturalis Biodiversity Center by a master's student and a lab technician (D3.1). I hope they will be completed by the end of the year. As we deviated from the initial question, we also incorporated morphometric and isotope data from the same specimens to examine whether adaptation results in genetic, morphological, and ecological divergence. Morphometric data has already been measured by PhD student Stephanie Martinez, while isotope analyses are being conducted by the master's student. Unfortunately, we cannot differentiate between males and females, as only fin clips were collected.

Transfer of knowledge: This working package has been part of two master theses (Stephanie Martinez and Istiuk Rubby) and in collaboration with Wageningen University and Naturalis Biodiversity Center. We presented our work plan to the government authorities in Indonesia BRIN and Papua and Bogor University, together with a knowledge-sharing workshop (D.5.3).

State of the art: This study provides an elegant and comprehensive demonstration of how the island-like conditions of marine lakes influence genetic, morphological, and ecological divergence. Focusing on the Puntang goby as a model organism offers valuable insights into the interplay between isolation and adaptation. Moreover, integrating genetic, morphometric, and isotope data is a novel approach that sheds light on the various genetic, morphological, and ecological aspects influencing adaptation in these unique environments. This research contributes to a deeper understanding of evolutionary processes in isolated environments, serving as a benchmark for future studies on adaptation in similar systems.
Corals and fish in marine lakes, Misool Island, Raja Ampat, Indonesia. Photo credits: Adriana Alzate
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