Elsevier

Progress in Oceanography

Volume 174, May–June 2019, Pages 7-16
Progress in Oceanography

Different ecological mechanisms lead to similar grazer controls on the functioning of periphyton Antarctic and sub-Antarctic communities

https://doi.org/10.1016/j.pocean.2018.01.008Get rights and content

Highlights

  • Grazing influences Antarctic and sub-Antarctic periphyton functioning.

  • The ecological mechanisms differ between both systems.

  • The mechanisms include grazer negative density dependence and niche partitioning.

Abstract

The processes underpinning the differences between Antarctic and sub-Antarctic ecological communities are still unclear. Dispersal, drift, speciation, and abiotic environmental filtering have been considered to explain these differences; biotic interactions, however, have received less attention. Antarctic intertidal assemblages of macrobenthic grazers are characterised by numerically abundant populations of a single species, Nacella concinna. In contrast, sub-Antarctic habitats display a diverse assemblage of herbivores like chitons, keyhole limpets, and several species of Nacella. Thus, it was hypothesised that herbivores would have significant density-dependent effects of a single species on benthic primary productivity in Antarctica, but stronger effects of the whole assemblage in the sub-Antarctic. Field grazer inclusion-exclusion experiments showed that chlorophyll-a (chl-a) concentration was one order of magnitude lower in Fildes Bay (King George Island, Antarctica) than in the Strait of Magellan (Chilean South Patagonia). Still, grazers had significant and negative effects on chl-a accrual, a proxy for productivity, in both sites. In Fildes Bay, these effects were similar between experimental levels or grazer density. Accordingly, evidence for negative density dependence of per capita interaction strength was detected in this region. In the Strait of Magellan, only the open access treatments, exposed to the diverse assemblage of grazers, significantly decreased chl-a accrual. Grazers negatively affected the relative abundance of browns (i.e. diatoms, dinoflagellates, and early stages of brown algae) and cyanobacteria at both sites, but favoured green algae and bare substratum in Fildes Bay and Strait of Magellan, respectively. These results suggest that different mechanisms, such as negative density dependence and resource partitioning, can lead to similar grazing controls of the productivity of Antarctic and sub-Antarctic periphyton communities. Herbivory should be incorporated as a local biotic filter into a comprehensive model of community structure and functioning for these ecosystems.

Introduction

Polar and sub-polar regions currently show the fastest responses to climate change on earth (e.g. Blunden et al., 2013). This scenario compels us to improve our mechanistic understanding of the structure and functioning of local natural communities in these regions (Kennicutt et al., 2014). In particular, explaining the differences and similarities between Antarctic and sub-Antarctic communities remains as a central aim of polar ecology (Kaiser et al., 2013). For example, dispersal and neutral stochasticity, two fundamental processes in the theory of island biogeography (MacArthur and Wilson, 1967), are suggested to explain the comparatively high diversity of marine intertidal species in King George Island (Griffiths and Waller, 2016). Selective pressure derived from nutrient inputs and glacier impacts has been suggested as a relevant factor reducing sub-Antarctic coastal diversity (e.g. Pugh and Davenport, 1997, Kim, 2001, Barnes et al., 2006). However, local biotic interactions, such as consumption, have received less attention in the quest for explaining ecological differences and similarities between both regions (McClintock et al., 2008, Amsler et al., 2012, Andrade and Brey, 2014, Chown et al., 2015). Coastal Antarctic and sub-Antarctic habitats harbour differing assemblages of macrobenthic consumers (Hogg et al., 2011, Griffiths and Waller, 2016), which can have contrasting effects on community structure and also on relevant ecosystem properties such as productivity, as shown in other regions of the world (Gamfeldt et al., 2015).

Herbivory is a key form of consumption with deterministic effects on ecosystem processes and community structure across latitudes, species pools, and abiotic conditions (e.g. Lubchenco and Gaines, 1981, Hawkins and Hartnoll, 1983, Coleman et al., 2006, Poore et al., 2012). Evidence from several latitudes indicates that grazing can explain, in part, broad-scale patterns of community structure (Coleman et al., 2006, Poore et al., 2012, Aguilera et al., 2016). For example, grazing by benthic intertidal gastropods can affect the range limit of primary producers, influencing their broader-scale distribution patterns (Aguilera et al., 2016). At the local scale, grazers have been shown to modify the spatiotemporal variability in the abundance of primary producers and invertebrates (Benedetti-Cecchi, 2000, Orostica et al., 2014, Tejada-Martinez et al., 2016). Importantly, herbivory impacts relevant ecosystem processes that account for the transferring of primary production outcomes to higher trophic levels in the food web (e.g. Gamfeldt et al., 2015). This consumptive interaction, therefore, might well constitute part of the local selective forces (i.e. a “biotic filter”; HilleRisLambers et al., 2012) that influence not only the structure, but also the functioning of coastal Antarctic and sub-Antarctic communities.

Ecosystem functions (or properties) are aggregate, emergent estimations that account for fluxes of energy, nutrients, and organic matter across a given environment (reviewed in Cardinale et al., 2012). These properties can be used to compare communities between regions characterised by different species pools and environmental conditions, like Antarctic and sub-Antarctic areas. Primary productivity is an example of ecosystem property, which can be represented as the accrual of chlorophyll-a (chl-a) over time. In the case of intertidal rocky-shore habitats, chl-a accrual of periphyton communities defines a key bottom-up input of energy that propagates through the assemblage (e.g. Bustamante et al., 1995, Hillebrand, 2003, Liess and Hillebrand, 2004). Functionally distinct macrobenthic grazers habiting species-rich rocky shores can have different effects on the structure of local periphyton communities (Aguilera et al., 2013), hinting at some degree of resource partitioning among these consumers. Accordingly, different assemblages of grazers from Antarctic and sub-Antarctic coastal communities might encompass different top-down forces, which in turn could drive broad-scale differences in chl-a accrual between these regions.

The diversity of grazers, and species in general, can have positive effects on resource use through niche partitioning (Duffy et al., 2017). In general, laboratory and field experiments demonstrate that resource use is less efficient in depauperate communities relative to speciose communities of consumers (O'Connor and Crowe, 2005, Griffin et al., 2009, Duffy et al., 2017), supporting predictions from niche theory (MacArthur and Levins, 1967, Lehman and Tilman, 2000). On Antarctic intertidal rocky-shores, dense populations of a single grazer species, Nacella concinna, dominate the macrobenthic assemblages (e.g. Valdivia et al., 2014). The populations of N. concinna have been demonstrated to have significant effects on periphyton and macroalgal communities (Kim, 2001), independently of abiotic environmental conditions such as varying UV radiation and air exposure (Zacher et al., 2007, Segovia-Rivera and Valdivia, 2016). In contrast, sub-Antarctic communities show a comparatively high diversity of macrograzers, which include chitons, keyhole limpets, and several Nacella spp. (Griffiths and Waller, 2016). According to the general consensus about the significant role of biodiversity in resource utilisation and ecosystem functioning (Griffin et al., 2009, Griffin et al., 2010, Cardinale et al., 2012), we could thus hypothesise that grazers would have significant density-dependent effects on periphyton community structure and productivity in Antarctica, but stronger effects of the species-rich assemblage in the sub-Antarctic region.

Here, we test the hypothesis that the differing levels of diversity between Antarctic and sub-Antarctic assemblages of macrograzers lead to different top-down controls of local periphyton productivity between both regions. From this hypothesis we deduce the predictions that, in Antarctic shores, larger densities of a single grazer species, N. concinna, will have stronger and more negative effects on chl-a accrual (Prediction 1); and, in sub-Antarctic shores, the entire assemblage of grazers would have stronger effects on chl-a accrual than a single species at varying densities (Prediction 2). These predictions were tested through field exclusion-inclusion experiments replicated in Fildes Bay (West Antarctic Peninsula) and Strait of Magellan (Chilean South Patagonia).

Section snippets

Study sites

The study was conducted in Fildes Bay, King George Island, Antarctica, and Strait of Magellan, Chilean South Patagonia. In each locality, we selected a wave-sheltered intertidal site that spanned ca. 100 m of the shore and was characterised by large benches of emergent rock (Fig. 1A and B). The experiments were set-up along the mid-low intertidal zone and were visited during diurnal low-tide hours. The studies were conducted between January and February 2017 in Fildes Bay, and between December

Results

Both sites harboured different densities of grazers along mid-low intertidal fringes. The density of N. concinna in Fildes Bay was, on average, 57% larger than the density of Nacella spp. in Strait of Magellan (Fig. 2A). Twelve taxa composed the grazer assemblage in Strait of Magellan, which was numerically dominated by N. deaurata (Fig. 2B). Daily maximum wave velocities in the study sites were comparable to those of wave-sheltered southern Pacific shores (e.g. Castilla et al., 1998), with

Discussion

The results of our study suggest that grazer assemblages from Antarctic and sub-Antarctic rocky shores exert different forms of top-down controls, but similar effects, on the functioning of benthic communities: whereas in Fildes Bay the experimental densities of N. concinna led to significant and similar reductions in chl-a accrual (a proxy for productivity), in Strait of Magellan the open access and control treatments, which allowed a species-rich grazer assemblage to access the experimental

Conclusion

In summary, our results suggest that grazer assemblages can have similar controlling effects on productivity and structure across Antarctic and sub-Antarctic benthic communities. The mechanisms underpinning these effects, interestingly, seem to differ functionally between both regions, with negative density-dependence and resource complementarity (and probably identity effects) likely relevant in the former and latter ecosystem, respectively. More research is needed to integrate the role of

Acknowledgements

This study was financially supported by FONDAP grant #15150003, Centro de Investigación en Dinámica de Ecosistemas Marinos de Altas Latitudes (IDEAL). While writing, NV was supported by FONDECYT grant #1141037. IG and PH acknowledge support from FONDECYT grant #1161129. Danielle Barriga improved the English style of an early version of the manuscript. We thank Dayane Yolette Osman and Juan Pablo Rodríguez for laboratory and field support. Stephen Hawkins and an anonymous reviewer provided

References (88)

  • D.K.A. Barnes et al.

    Shallow benthic fauna communities of South Georgia Island

    Polar Biol.

    (2006)
  • D. Bates et al.

    Fitting linear mixed-effects models using lme4

    J. Stat. Softw.

    (2015)
  • E.C. Bell et al.

    Quantifying “wave exposure”: a simple device for recording maximum velocity and results of its use at several field sites

    J. Exp. Mar. Biol. Ecol.

    (1994)
  • L. Benedetti-Cecchi

    Variance in ecological consumer-resource interactions

    Nature

    (2000)
  • L. Benedetti-Cecchi et al.

    Spatial distribution of algae and invertebrates in the rocky intertidal zone of the Strait of Magellan: are patterns general?

    Polar Biol.

    (1997)
  • E.L. Berlow et al.

    Quantifying variation in the strengths of species interactions

    Ecology

    (1999)
  • A.A. Berryman

    On principles, laws and theory in population ecology

    Oikos

    (2003)
  • J. Blunden et al.

    State of the climate in 2012

    Bull. Am. Meteorol. Soc.

    (2013)
  • D. Boaventura et al.

    Size matters: competition within populations of the limpet Patella depressa

    J. Anim. Ecol.

    (2003)
  • R.H. Bustamante et al.

    Gradients of intertidal primary productivity around the coast of South-Africa and their relationships with consumer biomass

    Oecologia

    (1995)
  • G.L. Campana et al.

    Drivers of colonization and succession in polar benthic macro- and microalgal communities

    Bot. Mar.

    (2009)
  • Canty, A., Ripley, B., 2016. Boot: Bootstrap R (S-Plus) Functions. R Package Version...
  • M.-J. Caramujo et al.

    Trophic interactions between benthic copepods and algal assemblages: a laboratory study

    J. North Am. Benthol. Soc.

    (2005)
  • B.J. Cardinale et al.

    Biodiversity loss and its impact on humanity

    Nature

    (2012)
  • J. Castilla et al.

    Quantifying wave exposure daily and hourly on the intertidal rocky shore of central Chile

    Rev. Chil. Hist. Nat.

    (1998)
  • P. Chesson

    Mechanisms of maintenance of species diversity

    Annu. Rev. Ecol. Syst.

    (2000)
  • S.L. Chown et al.

    The changing form of Antarctic biodiversity

    Nature

    (2015)
  • R.A. Christofoletti et al.

    Environmental and grazing influence on spatial variability of intertidal biofilm on subtropical rocky shores

    Mar. Ecol. Prog. Ser.

    (2011)
  • R.A. Coleman et al.

    A continental scale evaluation of the role of limpet grazing on rocky shores

    Oecologia

    (2006)
  • R.G. Creese et al.

    Analysis of interspecific and intraspecific competition amongst inter-tidal limpets with different methods of feeding

    Oecologia

    (1982)
  • A.C. Davison et al.

    Bootstrap Methods and Their Applications

    (1997)
  • P.K. Dayton

    The structure and regulation of some south-American kelp communities

    Ecol. Monogr.

    (1985)
  • Duffy, J.E., Godwin, C.M., Cardinale, B.J., 2017. Biodiversity effects in the wild are common and as strong as key...
  • J.E. Duffy et al.

    Biodiversity mediates top-down control in eelgrass ecosystems: a global comparative-experimental approach

    Ecol. Lett.

    (2015)
  • Ekstrøm, C., 2016. MESS: Miscellaneous Esoteric Statistical...
  • E. Fica et al.

    General spatial spectral variation in rocky intertidal communities from three biogeographical regions

    J. Biogeogr.

    (2017)
  • A.S. Flecker et al.

    Interactions between herbivorous fishes and limiting nutrients in a tropical stream ecosystem

    Ecology

    (2002)
  • L. Gamfeldt et al.

    Marine biodiversity and ecosystem functioning: what's known and what's next?

    Oikos

    (2015)
  • C.A. Gonzalez-Wevar et al.

    Concerted genetic, morphological and ecological diversification in Nacella limpets in the Magellanic Province

    Mol. Ecol.

    (2011)
  • J.N. Griffin et al.

    Predator diversity and ecosystem functioning: density modifies the effect of resource partitioning

    Ecology

    (2008)
  • J.N. Griffin et al.

    Spatial heterogeneity increases the importance of species richness for an ecosystem process

    Oikos

    (2009)
  • J.N. Griffin et al.

    Consumer effects on ecosystem functioning in rock pools: roles of species richness and composition

    Mar. Ecol. Prog. Ser.

    (2010)
  • H.J. Griffiths et al.

    The first comprehensive description of the biodiversity and biogeography of Antarctic and Sub-Antarctic intertidal communities

    J. Biogeogr.

    (2016)
  • S.J. Hawkins

    The influence of season and barnacles on the algal colonization of Patella vulgata exclusion areas

    J. Mar. Biol. Assoc. United Kingdom

    (1981)
  • Cited by (10)

    • Variability at multiple spatial scales in intertidal and subtidal macrobenthic communities in a fjord with glaciers, Magellanic Subantarctic ecoregion, Chile

      2022, Progress in Oceanography
      Citation Excerpt :

      Nacella species have been described as forcing the richness and abundance of algae, as well as structuring the intertidal macro and microalgal communities (Aguilera, 2011, Valdivia et al., 2014, Valdivia et al., 2018). However, in our study N. magellanica was present with minimal abundances in the FMO, rejecting herbivory as an ecological process that is structuring and modifying the spatial patterns of algal communities along the FMO (Rosenfeld et al., 2018, Valdivia et al., 2018). Therefore, our results differ from those found by Valdivia et al. (2014) where the high abundance of the grazer N. concinna would be forcing the structuring and formation of vertical and horizontal patterns of spatial variability at small scales in the intertidal communities of King George Island, Antarctica.

    • Latitudinal changes in the trophic structure of benthic coastal food webs along the Antarctic Peninsula

      2021, Marine Environmental Research
      Citation Excerpt :

      Conversely, the herbivorous limpet N. concinna was at all sites highly enriched in 13C and hence, more likely to rely on coralline encrusting algae than on canopy-forming macroalgae such as H. grandifolius or Desmarestia spp. Similar results have been reported elsewhere indicating a diet based on microphytobenthos or intertidal macroalgae (Corbisier et al., 2004; Choy et al., 2011; Daglio et al., 2018; Zenteno et al., 2019; Valdivia et al., 2019), although some related species from Patagonia are best described as omnivores (Andrade and Brey 2014). The snail M. antarctica was a carnivore highly positioned in the food web at the five sites studied, although it has been reported previously to be a herbivore (Gutt and Schickan 1998; Amsler et al., 2019; Michel et al., 2019) and was here sometimes found crawling on macroalgae, likely suggesting this species grazes on animal epiphytes.

    View all citing articles on Scopus
    View full text