Seasonality elicits herbivores' escape from trophic control and favors induced resistance in a temperate macroalga

Haavisto, Fiia; Jormalainen, Veijo

doi:10.1890/13-2387.1

Cited by 23 publications

(15 citation statements)

References 64 publications

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“…If F. vesiculosus goes extinct or becomes rarer in the Bothnian Sea, the empty habitat left along the rocky shores may provide extra littoral habitat and settlement substrate for F. radicans. The mesograzer I. balthica is the main grazer of Baltic Sea fucoids (Jormalainen and Ramsay 2009, Haavisto and Jormalainen 2014. Where both Fucus species co-exist, I. balthica is more abundant on F. radicans, which it prefers over F. vesiculosus in choice experiments ).…”

Section: Discussionmentioning

confidence: 98%

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Tolerance to climate change of the clonally reproducing endemic Baltic seaweed, Fucus radicans: is phenotypic plasticity enough?

Rugiu

Manninen

Rothäusler

et al. 2018

Journal of Phycology

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To predict the effects of climate change, we first need information on both the current tolerance ranges of species and their future adaptive potential. Adaptive responses may originate either in genetic variation or in phenotypic plasticity, but the relative importance of these factors is poorly understood. Here, we tested the tolerance of Fucus radicans to the combination of hyposalinity and warming projected by climate models for 2070–2099. We measured the growth and survival responses of thalli in both current and future conditions, focusing on variations in tolerance among and within different clonal lineages. Survival was 32% lower in future than in current conditions, but the weight and length of the thalli which survived was respectively 267% and 178% higher when exposed to future conditions. The relatively high tolerance to the future conditions suggests that F. radicans is likely to persist in its current distributional range, which is limited to the Gulf of Bothia and Estonian coast in the Baltic Sea. Furthermore, this species may be able to expand its distribution southward and replace its congener F. vesiculosus, which, in previous studies, has not tolerated the future conditions as well. In addition, we discovered variation in tolerance to future conditions within one of the clonal lineages, which have been hitherto presumed to lack adaptive variation. The discovery of intra‐clonal phenotypic plasticity means that this alga has the potential for adaptive responses to climate change, which may be the key to the future persistence of F. radicans in the Baltic Sea.

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Section: Discussionmentioning

confidence: 98%

“…The mesograzer I. balthica is the main grazer of Baltic Sea fucoids (Jormalainen and Ramsay , Forslund et al. , Haavisto and Jormalainen ). Where both Fucus species co‐exist, I. balthica is more abundant on F. radicans , which it prefers over F. vesiculosus in choice experiments (Forslund et al.…”

Section: Discussionmentioning

confidence: 99%

Tolerance to climate change of the clonally reproducing endemic Baltic seaweed, Fucus radicans: is phenotypic plasticity enough?

Rugiu

Manninen

Rothäusler

et al. 2018

Journal of Phycology

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“…We suggest this was due to the increasing magnitude of topdown regulation of periphyton later in the season when the invertebrate grazer densities are peaking. In the highly seasonal environment of the Northern Baltic Sea, grazer densities on F. vesiculosus thalli are multifold in autumn after a reproductive period during summer (Korpinen et al 2010, Haavisto andJormalainen 2014). Herbivory on periphyton is generally high in coastal ecosystems as grazers may remove up to an average of 60% of the periphyton biomass as well as affect its spatial distribution and decrease species richness (Hillebrand et al 2000, Hillebrand 2008).…”

Section: Discussionmentioning

confidence: 99%

Genetic variation of a foundation rockweed species affects associated communities

Jormalainen

Danelli

Gagnon

et al. 2017

Ecology

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Genetic variation in a foundation species may affect the composition of associated communities as well as modify ecosystem function. While the ecological consequences of genetic diversity of foundation species have been widely reported, the ability of individual genotypes to support dissimilar communities has been documented only in forest ecosystems. Here, for the first time in a marine ecosystem, we test whether the different genotypes of the rockweed Fucus vesiculosus harbor distinct community phenotypes and whether the genetic similarity of individual genotypes or their defensive compound content can explain the variation of the associated communities. We reared replicated genotypes in a common garden in the sea and analyzed their associated communities of periphytic algae and invertebrates as well as determined their contents of defense compounds, phlorotannins, and genetic distance based on neutral molecular markers. The periphytic community was abundant in mid-summer and its biovolume, diversity and community composition varied among the rockweed genotypes. The diversity of the periphytic community decreased with its increasing biovolume. In autumn, when grazers were abundant, periphytic community biomass was lower and less variable among rockweed genotypes, indicating different relative importance of bottom-up regulation through heritable variation of the foundation species and top-down regulation through grazing intensity. Similarly, composition of the invertebrate community varied among the rockweed genotypes. Although the genotype explained about 10-18% of the variation in associated communities, the variation was explained neither by the genetic distance nor the phlorotannin content. Thus, neither neutral genetic markers nor a single phenotypic trait could provide a mechanistic understanding of the genetic basis of community specificity. Therefore, a more comprehensive mapping of quantitative trait variation is needed to understand the underlying mechanisms. The community specificity implies that genetic variation within a foundation species is crucial for the biodiversity and assembly of associated organisms and, thus, for the functioning of associated communities. The result highlights the importance of ensuring the genetic variation of foundation species as a conservation target.

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“…Such plasticity allows primary producers to adapt to spatially or temporally variable environments, while reducing costs of constantly expressing these induced traits (Bradshaw 1965, Dudley and Schmitt 1996, Padilla and Savedo 2013, Murren et al 2015. Although there is substantial evidence that induced resistance can vary with environmental conditions (Lou andBaldwin 2004, Weinberger et al 2011), spatial or temporal differences in grazing pressure (Long and Trussell 2007, Long et al 2011, Haavisto and Jormalainen 2014, Wieski and Pennings 2014, or genotype (Karban and Baldwin 1997, Underwood 2000, Agrawal et al 2002, Haavisto et al 2010, Holeski et al 2010, Haavisto and Jormalainen 2014, we still have a limited understanding of how variable these traits may be within a species, particularly for marine plants and seaweeds. Because competition between herbivores is often mediated by changes in primary producer phenotype, intraspecific variation in resistance may have important implications for regulating herbivore community composition and function (Agrawal 2005, Poelman et al 2008.…”

Section: Introductionmentioning

confidence: 99%

Geographic variation in the sensitivity of an herbivore‐induced seaweed defense

Jones

Long

2018

Ecology

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Intraspecific variation in primary producer induced defenses may affect how these defenses contribute to population and community regulation. For instance, inducible defenses may play larger roles in primary producer populations that are sensitive to low levels of grazing than populations that only respond to high levels of grazing. Although the incidence of herbivore-induced defenses is well documented, and there are examples of geographic variation in these defenses, we have limited knowledge of the factors that affect sensitivity to grazing (i.e., the minimum grazer density needed to elicit these responses) within and among populations. Filling this gap is necessary to understand the importance of these defenses under different conditions. To address whether the sensitivity of seaweed induced defenses varies geographically, we exposed Northern and Southern California populations of the seaweed Silvetia compressa to five densities of the snail Tegula funebralis, under ambient, regional environmental conditions. Southern seaweeds required high levels of grazing to induce defenses, while all levels of herbivory decreased Northern seaweed palatability. To better understand these different responses to low levels of grazing, we conducted common garden experiments to directly test the roles of experimental environment and herbivore source. Consistent with initial experiments, Northern Silvetia responded to low levels of grazing, regardless of environmental conditions, while Southern Silvetia never responded to low levels of grazing, even after being acclimated to Northern environmental conditions for 24 d. Additionally, Southern Silvetia did not respond to grazing by Northern snails, suggesting that herbivore source did not explain this geographic pattern in inducible seaweed defenses. Together, these observations suggest that the seaweed source explains this geographic pattern in sensitivity. Trade-offs with constitutive defenses did not help explain this pattern, as Southern Silvetia had weaker constitutive defenses than Northern seaweeds. This may be due to a combination of low grazing pressure and low predictability of attack in the South. Thus, population variation in sensitivity may be due to long-term differences in environmental histories, resulting in local adaptation or legacy effects from exposure to local conditions. Overall, our results indicate that these herbivore-induced responses may be more important in Northern Silvetia populations than Southern ones.

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Seasonality elicits herbivores' escape from trophic control and favors induced resistance in a temperate macroalga

Cited by 23 publications

References 64 publications

Tolerance to climate change of the clonally reproducing endemic Baltic seaweed, Fucus radicans: is phenotypic plasticity enough?

Tolerance to climate change of the clonally reproducing endemic Baltic seaweed, Fucus radicans: is phenotypic plasticity enough?

Genetic variation of a foundation rockweed species affects associated communities

Geographic variation in the sensitivity of an herbivore‐induced seaweed defense

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