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      Sun Compass Orientation Helps Coral Reef Fish Larvae Return to Their Natal Reef

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          Abstract

          Reef fish sustain populations on isolated reefs and show genetic diversity between nearby reefs even though larvae of many species are swept away from the natal site during pelagic dispersal. Retention or recruitment to natal reefs requires orientation capabilities that enable larvae to find their way. Although olfactory and acoustically based orientation has been implicated in homing when larvae are in the reef’s vicinity, it is still unclear how they cope with greater distances. Here we show evidence for a sun compass mechanism that can bring the larvae to the vicinity of their natal reef. In a circular arena, pre-settlement larvae and early settlers (<24 hours) of the cardinal fish, Ostorhinchus doederleini, showed a strong SSE directional swimming response, which most likely has evolved to compensate for the locally prevailing large scale NNW current drift. When fish were clock-shifted 6 hours, they changed their orientation by ca. 180° as predicted by the tropical sun curve at One Tree Island, i.e. they used a time-compensated sun compass. Furthermore, the fish oriented most consistently at times of the day when the sun azimuth is easy to determine. Microsatellite markers showed that the larvae that had just arrived at One Tree Island genetically belonged to either the local reef population or to Fitzroy Reef located 12 kilometers to the SSE. The use of a sun compass adds a missing long-distance link to the hierarchy of other sensory abilities that can direct larvae to the region of origin, including their natal reef. Predominant local recruitment, in turn, can contribute to genetic isolation and potential speciation.

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          Most cited references15

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          Detecting immigration by using multilocus genotypes.

          Immigration is an important force shaping the social structure, evolution, and genetics of populations. A statistical method is presented that uses multilocus genotypes to identify individuals who are immigrants, or have recent immigrant ancestry. The method is appropriate for use with allozymes, microsatellites, or restriction fragment length polymorphisms (RFLPs) and assumes linkage equilibrium among loci. Potential applications include studies of dispersal among natural populations of animals and plants, human evolutionary studies, and typing zoo animals of unknown origin (for use in captive breeding programs). The method is illustrated by analyzing RFLP genotypes in samples of humans from Australian, Japanese, New Guinean, and Senegalese populations. The test has power to detect immigrant ancestors, for these data, up to two generations in the past even though the overall differentiation of allele frequencies among populations is low.
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            Local replenishment of coral reef fish populations in a marine reserve.

            The scale of larval dispersal of marine organisms is important for the design of networks of marine protected areas. We examined the fate of coral reef fish larvae produced at a small island reserve, using a mass-marking method based on maternal transmission of stable isotopes to offspring. Approximately 60% of settled juveniles were spawned at the island, for species with both short ( 1 month) pelagic larval durations. If natal homing of larvae is a common life-history strategy, the appropriate spatial scales for the management and conservation of coral reefs are likely to be much smaller than previously assumed.
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              Smelling home can prevent dispersal of reef fish larvae.

              Many marine fish and invertebrates show a dual life history where settled adults produce dispersing larvae. The planktonic nature of the early larval stages suggests a passive dispersal model where ocean currents would quickly cause panmixis over large spatial scales and prevent isolation of populations, a prerequisite for speciation. However, high biodiversity and species abundance in coral reefs contradict this panmixis hypothesis. Although ocean currents are a major force in larval dispersal, recent studies show far greater retention than predicted by advection models. We investigated the role of animal behavior in retention and homing of coral reef fish larvae resulting in two important discoveries: (i) Settling larvae are capable of olfactory discrimination and prefer the odor of their home reef, thereby demonstrating to us that nearby reefs smell different. (ii) Whereas one species showed panmixis as predicted from our advection model, another species showed significant genetic population substructure suggestive of strong homing. Thus, the smell of reefs could allow larvae to choose currents that return them to reefs in general and natal reefs in particular. As a consequence, reef populations can develop genetic differences that might lead to reproductive isolation.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, USA )
                1932-6203
                2013
                26 June 2013
                : 8
                : 6
                : e66039
                Affiliations
                [1 ]Institut für Biologie und Umweltwissenschaften, Carl-von-Ossietzky Universität Oldenburg, Oldenburg, Germany
                [2 ]Forschungszentrum Neurosensorik, University of Oldenburg, Oldenburg, Germany
                [3 ]Boston University Marine Program, Boston, Massachusetts, United States of America
                [4 ]School of Marine and Tropical Biology and ARC Centre of Excellence for Coral Reef Studies, James Cook University, Townsville, Queensland, Australia
                Lund University, Sweden
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                Conceived and designed the experiments: HM GG. Performed the experiments: HM GG. Analyzed the data: HM GG JA MJK. Contributed reagents/materials/analysis tools: HM GG JA MJK. Wrote the paper: HM GG JA MJK.

                Article
                PONE-D-13-07953
                10.1371/journal.pone.0066039
                3694079
                23840396
                27aeecef-4fb8-4129-8c57-d922c31084f8
                Copyright @ 2013

                This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 22 February 2013
                : 1 May 2013
                Page count
                Pages: 9
                Funding
                This work was funded by a Lichtenberg professorship from the Volkswagen Stiftung to HM; DFG Ge842/6-1 to GG; Grant no. 7236-02, ARC grants, and funding from the ARC Centre of Excellence for Coral Reef Studies to MJK. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Biology
                Ecology
                Marine Ecology
                Coral Reefs
                Biodiversity
                Marine Biology
                Marine Ecology
                Neuroscience
                Behavioral Neuroscience
                Sensory Perception
                Sensory Systems
                Zoology
                Animal Behavior
                Ichthyology
                Earth Sciences
                Marine and Aquatic Sciences
                Marine Ecology

                Uncategorized
                Uncategorized

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