Limits...
Not just who, but how many: the importance of partner abundance in reef coral symbioses.

Cunning R, Baker AC - Front Microbiol (2014)

Bottom Line: The performance and function of reef corals depends on the genetic identity of their symbiotic algal partners, with some symbionts providing greater benefits (e.g., photosynthate, thermotolerance) than others.We suggest that symbiont abundance is a fundamental aspect of the dynamic interface between reef corals and the abiotic environment that ultimately determines the benefits, costs, and functional responses of these symbioses.In this article, we generate testable hypotheses regarding the importance of symbiont abundance by first discussing different metrics and their potential links to symbiosis performance and breakdown, and then describing how natural variability and dynamics of symbiont communities may help explain ecological patterns on coral reefs and predict responses to environmental change.

View Article: PubMed Central - PubMed

Affiliation: Department of Marine Biology and Ecology, Rosenstiel School of Marine and Atmospheric Science, University of Miami Miami, FL, USA.

ABSTRACT
The performance and function of reef corals depends on the genetic identity of their symbiotic algal partners, with some symbionts providing greater benefits (e.g., photosynthate, thermotolerance) than others. However, these interaction outcomes may also depend on partner abundance, with differences in the total number of symbionts changing the net benefit to the coral host, depending on the particular environmental conditions. We suggest that symbiont abundance is a fundamental aspect of the dynamic interface between reef corals and the abiotic environment that ultimately determines the benefits, costs, and functional responses of these symbioses. This density-dependent framework suggests that corals may regulate the size of their symbiont pool to match microhabitat-specific optima, which may contribute to the high spatiotemporal variability in symbiont abundance observed within and among colonies and reefs. Differences in symbiont standing stock may subsequently explain variation in energetics, growth, reproduction, and stress susceptibility, and may mediate the impacts of environmental change on these outcomes. However, the importance of symbiont abundance has received relatively little recognition, possibly because commonly-used metrics based on surface area (e.g., symbiont cells cm(-2)) may be only weakly linked to biological phenomena and are difficult to compare across studies. We suggest that normalizing symbionts to biological host parameters, such as units of protein or numbers of host cells, will more clearly elucidate the functional role of symbiont abundance in reef coral symbioses. In this article, we generate testable hypotheses regarding the importance of symbiont abundance by first discussing different metrics and their potential links to symbiosis performance and breakdown, and then describing how natural variability and dynamics of symbiont communities may help explain ecological patterns on coral reefs and predict responses to environmental change.

No MeSH data available.


Related in: MedlinePlus

Coral tissue architecture and different metrics of symbiont abundance. Two scenarios of coral and symbiont tissue architecture are shown, theoretically representing coral tissues in winter (A) and summer (B), with corresponding values of the symbiont to host cell ratio and areal symbiont density. Black rounded rectangles represent coral host cells (comprising ectoderm and endoderm tissue layers) and brown circles represent symbiont cells. Areal symbiont density is higher in (A), while the symbiont to host cell ratio is higher in (B), showing how these metrics may change in opposite ways depending on tissue architecture. Schematics are not to scale and are meant to illustrate conceptual differences between different metrics.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
getmorefigures.php?uid=PMC4120693&req=5

Figure 1: Coral tissue architecture and different metrics of symbiont abundance. Two scenarios of coral and symbiont tissue architecture are shown, theoretically representing coral tissues in winter (A) and summer (B), with corresponding values of the symbiont to host cell ratio and areal symbiont density. Black rounded rectangles represent coral host cells (comprising ectoderm and endoderm tissue layers) and brown circles represent symbiont cells. Areal symbiont density is higher in (A), while the symbiont to host cell ratio is higher in (B), showing how these metrics may change in opposite ways depending on tissue architecture. Schematics are not to scale and are meant to illustrate conceptual differences between different metrics.

Mentions: Differences among these metrics are likely the result of a dynamic vs. fixed quantity in the denominator. When symbionts are normalized to a dynamic unit (host protein, cells, etc.), their abundance is also influenced by changes in these units. Therefore, changes in coral tissue architecture may produce different patterns in different metrics of symbiont abundance (Figure 1). For example, as environmental conditions change from winter into summer, coral tissues become thinner (Barnes and Lough, 1992; Brown et al., 1999; Fitt et al., 2000; Thornhill et al., 2011), which may involve a loss of both symbiont and host cells on an areal basis. Decreased heterotrophy in summer (Ferrier-Pagès et al., 2011) may also reduce numbers of host prey-capture cells such as cnidocytes and mucocytes, but increased reproduction in summer may increase the number of host gametocytes and mesenterial cells. Higher summer temperatures may also increase respiration and host cell catabolism. Changes in cellular architecture as a result of these processes (e.g., Figures 1A,B) might lead to a greater net loss of host cells relative to symbionts, resulting in a reduction in symbionts per cm2, but an increase in the S/H cell ratio (Figure 1). Indeed, areal symbiont density tends to decrease in the summer (Stimson, 1997; Brown et al., 1999; Fagoonee et al., 1999; Fitt et al., 2000), while the S/H cell ratio may increase (Cunning and Baker, 2013).


Not just who, but how many: the importance of partner abundance in reef coral symbioses.

Cunning R, Baker AC - Front Microbiol (2014)

Coral tissue architecture and different metrics of symbiont abundance. Two scenarios of coral and symbiont tissue architecture are shown, theoretically representing coral tissues in winter (A) and summer (B), with corresponding values of the symbiont to host cell ratio and areal symbiont density. Black rounded rectangles represent coral host cells (comprising ectoderm and endoderm tissue layers) and brown circles represent symbiont cells. Areal symbiont density is higher in (A), while the symbiont to host cell ratio is higher in (B), showing how these metrics may change in opposite ways depending on tissue architecture. Schematics are not to scale and are meant to illustrate conceptual differences between different metrics.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4120693&req=5

Figure 1: Coral tissue architecture and different metrics of symbiont abundance. Two scenarios of coral and symbiont tissue architecture are shown, theoretically representing coral tissues in winter (A) and summer (B), with corresponding values of the symbiont to host cell ratio and areal symbiont density. Black rounded rectangles represent coral host cells (comprising ectoderm and endoderm tissue layers) and brown circles represent symbiont cells. Areal symbiont density is higher in (A), while the symbiont to host cell ratio is higher in (B), showing how these metrics may change in opposite ways depending on tissue architecture. Schematics are not to scale and are meant to illustrate conceptual differences between different metrics.
Mentions: Differences among these metrics are likely the result of a dynamic vs. fixed quantity in the denominator. When symbionts are normalized to a dynamic unit (host protein, cells, etc.), their abundance is also influenced by changes in these units. Therefore, changes in coral tissue architecture may produce different patterns in different metrics of symbiont abundance (Figure 1). For example, as environmental conditions change from winter into summer, coral tissues become thinner (Barnes and Lough, 1992; Brown et al., 1999; Fitt et al., 2000; Thornhill et al., 2011), which may involve a loss of both symbiont and host cells on an areal basis. Decreased heterotrophy in summer (Ferrier-Pagès et al., 2011) may also reduce numbers of host prey-capture cells such as cnidocytes and mucocytes, but increased reproduction in summer may increase the number of host gametocytes and mesenterial cells. Higher summer temperatures may also increase respiration and host cell catabolism. Changes in cellular architecture as a result of these processes (e.g., Figures 1A,B) might lead to a greater net loss of host cells relative to symbionts, resulting in a reduction in symbionts per cm2, but an increase in the S/H cell ratio (Figure 1). Indeed, areal symbiont density tends to decrease in the summer (Stimson, 1997; Brown et al., 1999; Fagoonee et al., 1999; Fitt et al., 2000), while the S/H cell ratio may increase (Cunning and Baker, 2013).

Bottom Line: The performance and function of reef corals depends on the genetic identity of their symbiotic algal partners, with some symbionts providing greater benefits (e.g., photosynthate, thermotolerance) than others.We suggest that symbiont abundance is a fundamental aspect of the dynamic interface between reef corals and the abiotic environment that ultimately determines the benefits, costs, and functional responses of these symbioses.In this article, we generate testable hypotheses regarding the importance of symbiont abundance by first discussing different metrics and their potential links to symbiosis performance and breakdown, and then describing how natural variability and dynamics of symbiont communities may help explain ecological patterns on coral reefs and predict responses to environmental change.

View Article: PubMed Central - PubMed

Affiliation: Department of Marine Biology and Ecology, Rosenstiel School of Marine and Atmospheric Science, University of Miami Miami, FL, USA.

ABSTRACT
The performance and function of reef corals depends on the genetic identity of their symbiotic algal partners, with some symbionts providing greater benefits (e.g., photosynthate, thermotolerance) than others. However, these interaction outcomes may also depend on partner abundance, with differences in the total number of symbionts changing the net benefit to the coral host, depending on the particular environmental conditions. We suggest that symbiont abundance is a fundamental aspect of the dynamic interface between reef corals and the abiotic environment that ultimately determines the benefits, costs, and functional responses of these symbioses. This density-dependent framework suggests that corals may regulate the size of their symbiont pool to match microhabitat-specific optima, which may contribute to the high spatiotemporal variability in symbiont abundance observed within and among colonies and reefs. Differences in symbiont standing stock may subsequently explain variation in energetics, growth, reproduction, and stress susceptibility, and may mediate the impacts of environmental change on these outcomes. However, the importance of symbiont abundance has received relatively little recognition, possibly because commonly-used metrics based on surface area (e.g., symbiont cells cm(-2)) may be only weakly linked to biological phenomena and are difficult to compare across studies. We suggest that normalizing symbionts to biological host parameters, such as units of protein or numbers of host cells, will more clearly elucidate the functional role of symbiont abundance in reef coral symbioses. In this article, we generate testable hypotheses regarding the importance of symbiont abundance by first discussing different metrics and their potential links to symbiosis performance and breakdown, and then describing how natural variability and dynamics of symbiont communities may help explain ecological patterns on coral reefs and predict responses to environmental change.

No MeSH data available.


Related in: MedlinePlus