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Phenotypic variation and fitness in a metapopulation of tubeworms (Ridgeia piscesae Jones) at hydrothermal vents.

Tunnicliffe V, St Germain C, Hilário A - PLoS ONE (2014)

Bottom Line: This foundation species at northeast Pacific hydrothermal sites occupies a wide habitat range in a highly heterogeneous environment.Although only the largest worms were measured, only 17% of low flux worms were reproductively competent compared to 91% of high flux worms.This foundation species forms a metapopulation with variable growth characteristics in a heterogeneous environment where a strategy of phenotypic variation bestows an advantage over specialization.

View Article: PubMed Central - PubMed

Affiliation: Department of Biology, University of Victoria, Victoria, British Columbia, Canada; School of Earth & Ocean Sciences, University of Victoria, Victoria, British Columbia, Canada.

ABSTRACT
We examine the nature of variation in a hot vent tubeworm, Ridgeia piscesae, to determine how phenotypes are maintained and how reproductive potential is dictated by habitat. This foundation species at northeast Pacific hydrothermal sites occupies a wide habitat range in a highly heterogeneous environment. Where fluids supply high levels of dissolved sulphide for symbionts, the worm grows rapidly in a "short-fat" phenotype characterized by lush gill plumes; when plumes are healthy, sperm package capture is higher. This form can mature within months and has a high fecundity with continuous gamete output and a lifespan of about three years in unstable conditions. Other phenotypes occupy low fluid flux habitats that are more stable and individuals grow very slowly; however, they have low reproductive readiness that is hampered further by small, predator cropped branchiae, thus reducing fertilization and metabolite uptake. Although only the largest worms were measured, only 17% of low flux worms were reproductively competent compared to 91% of high flux worms. A model of reproductive readiness illustrates that tube diameter is a good predictor of reproductive output and that few low flux worms reached critical reproductive size. We postulate that most of the propagules for the vent fields originate from the larger tubeworms that live in small, unstable habitat patches. The large expanses of worms in more stable low flux habitat sustain a small, but long-term, reproductive output. Phenotypic variation is an adaptation that fosters both morphological and physiological responses to differences in chemical milieu and predator pressure. This foundation species forms a metapopulation with variable growth characteristics in a heterogeneous environment where a strategy of phenotypic variation bestows an advantage over specialization.

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Ridgeia piscesae on Juan de Fuca Ridge.Images taken using the vehicle ROPOS (Canadian Scientific Submersible Facility).A. Eight months post-eruption at Nascent Vent, South Rift Zone, Axial; scale 10 cm. B. Branchial plume with white obturaculum of high flux R. piscesae; scale 1.5 cm. C. Sparse branchial plumes in low flux grazed by polynoid polychaetes (top centre); scale 1.5 cm. D. Clump of short-fat R. piscesae on the side of a smoker chimney; fluids emerging from ledge below. Orange polychaetes are Paralvinella palmiformis, a microbial grazer; scale 5 cm. E. Extensive tubeworm clumps on basalts in weak fluid flow between chimneys; image about 2 m across.
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pone-0110578-g003: Ridgeia piscesae on Juan de Fuca Ridge.Images taken using the vehicle ROPOS (Canadian Scientific Submersible Facility).A. Eight months post-eruption at Nascent Vent, South Rift Zone, Axial; scale 10 cm. B. Branchial plume with white obturaculum of high flux R. piscesae; scale 1.5 cm. C. Sparse branchial plumes in low flux grazed by polynoid polychaetes (top centre); scale 1.5 cm. D. Clump of short-fat R. piscesae on the side of a smoker chimney; fluids emerging from ledge below. Orange polychaetes are Paralvinella palmiformis, a microbial grazer; scale 5 cm. E. Extensive tubeworm clumps on basalts in weak fluid flow between chimneys; image about 2 m across.

Mentions: New vents created by the eruption were emitting fluids over 20°C with substantial levels of dissolved sulphide (Table S1) while surviving vents were cooler. In general, there is more sulphide at higher temperatures, a relationship evident across a much wider suite of samples at Axial [34]. In the following two years, heat and sulphide levels dropped as the volcano cooled. In the first year, tubeworms at these new vents were fatter and shorter than the older animals in less vigorous flow (Figure 2A). Settling larvae recruited and grew to 23 cm length within 280 days (Figure 3A) at which time, of 59 animals, 60% were already producing gametes. In the following two years as sulphide flux diminished somewhat, growth remained vigorous (at a minimum of 50 cm/yr) but the tube form elongate greatly (Figure 2B). As tubes lengthened, so did the trunk (r2 = 0.96, n = 57). One collection at Nascent Vent in 2001 revealed that all long worms had died and empty tube surfaces hosted a second generation of recruits over 30 cm long. The first generation lasted three years.


Phenotypic variation and fitness in a metapopulation of tubeworms (Ridgeia piscesae Jones) at hydrothermal vents.

Tunnicliffe V, St Germain C, Hilário A - PLoS ONE (2014)

Ridgeia piscesae on Juan de Fuca Ridge.Images taken using the vehicle ROPOS (Canadian Scientific Submersible Facility).A. Eight months post-eruption at Nascent Vent, South Rift Zone, Axial; scale 10 cm. B. Branchial plume with white obturaculum of high flux R. piscesae; scale 1.5 cm. C. Sparse branchial plumes in low flux grazed by polynoid polychaetes (top centre); scale 1.5 cm. D. Clump of short-fat R. piscesae on the side of a smoker chimney; fluids emerging from ledge below. Orange polychaetes are Paralvinella palmiformis, a microbial grazer; scale 5 cm. E. Extensive tubeworm clumps on basalts in weak fluid flow between chimneys; image about 2 m across.
© Copyright Policy
Related In: Results  -  Collection

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getmorefigures.php?uid=PMC4206443&req=5

pone-0110578-g003: Ridgeia piscesae on Juan de Fuca Ridge.Images taken using the vehicle ROPOS (Canadian Scientific Submersible Facility).A. Eight months post-eruption at Nascent Vent, South Rift Zone, Axial; scale 10 cm. B. Branchial plume with white obturaculum of high flux R. piscesae; scale 1.5 cm. C. Sparse branchial plumes in low flux grazed by polynoid polychaetes (top centre); scale 1.5 cm. D. Clump of short-fat R. piscesae on the side of a smoker chimney; fluids emerging from ledge below. Orange polychaetes are Paralvinella palmiformis, a microbial grazer; scale 5 cm. E. Extensive tubeworm clumps on basalts in weak fluid flow between chimneys; image about 2 m across.
Mentions: New vents created by the eruption were emitting fluids over 20°C with substantial levels of dissolved sulphide (Table S1) while surviving vents were cooler. In general, there is more sulphide at higher temperatures, a relationship evident across a much wider suite of samples at Axial [34]. In the following two years, heat and sulphide levels dropped as the volcano cooled. In the first year, tubeworms at these new vents were fatter and shorter than the older animals in less vigorous flow (Figure 2A). Settling larvae recruited and grew to 23 cm length within 280 days (Figure 3A) at which time, of 59 animals, 60% were already producing gametes. In the following two years as sulphide flux diminished somewhat, growth remained vigorous (at a minimum of 50 cm/yr) but the tube form elongate greatly (Figure 2B). As tubes lengthened, so did the trunk (r2 = 0.96, n = 57). One collection at Nascent Vent in 2001 revealed that all long worms had died and empty tube surfaces hosted a second generation of recruits over 30 cm long. The first generation lasted three years.

Bottom Line: This foundation species at northeast Pacific hydrothermal sites occupies a wide habitat range in a highly heterogeneous environment.Although only the largest worms were measured, only 17% of low flux worms were reproductively competent compared to 91% of high flux worms.This foundation species forms a metapopulation with variable growth characteristics in a heterogeneous environment where a strategy of phenotypic variation bestows an advantage over specialization.

View Article: PubMed Central - PubMed

Affiliation: Department of Biology, University of Victoria, Victoria, British Columbia, Canada; School of Earth & Ocean Sciences, University of Victoria, Victoria, British Columbia, Canada.

ABSTRACT
We examine the nature of variation in a hot vent tubeworm, Ridgeia piscesae, to determine how phenotypes are maintained and how reproductive potential is dictated by habitat. This foundation species at northeast Pacific hydrothermal sites occupies a wide habitat range in a highly heterogeneous environment. Where fluids supply high levels of dissolved sulphide for symbionts, the worm grows rapidly in a "short-fat" phenotype characterized by lush gill plumes; when plumes are healthy, sperm package capture is higher. This form can mature within months and has a high fecundity with continuous gamete output and a lifespan of about three years in unstable conditions. Other phenotypes occupy low fluid flux habitats that are more stable and individuals grow very slowly; however, they have low reproductive readiness that is hampered further by small, predator cropped branchiae, thus reducing fertilization and metabolite uptake. Although only the largest worms were measured, only 17% of low flux worms were reproductively competent compared to 91% of high flux worms. A model of reproductive readiness illustrates that tube diameter is a good predictor of reproductive output and that few low flux worms reached critical reproductive size. We postulate that most of the propagules for the vent fields originate from the larger tubeworms that live in small, unstable habitat patches. The large expanses of worms in more stable low flux habitat sustain a small, but long-term, reproductive output. Phenotypic variation is an adaptation that fosters both morphological and physiological responses to differences in chemical milieu and predator pressure. This foundation species forms a metapopulation with variable growth characteristics in a heterogeneous environment where a strategy of phenotypic variation bestows an advantage over specialization.

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