Advertisement
Browse Subject Areas
?

Click through the PLOS taxonomy to find articles in your field.

For more information about PLOS Subject Areas, click here.

  • Loading metrics

Benthic meiofaunal community response to the cascading effects of herbivory within an algal halo system of the Great Barrier Reef

  • Quinn R. Ollivier ,

    Roles Data curation, Formal analysis, Investigation, Methodology, Writing – original draft

    Q.Ollivier@deakin.edu.au

    Affiliations Centre for Integrative Ecology, School of Life and Environmental Sciences, Faculty of Science Engineering and Built Environment, Deakin University, Melbourne, VIC, Australia, School of Life Sciences, University of Technology Sydney, Sydney, NSW, Australia

  • Edward Hammill,

    Roles Conceptualization, Funding acquisition, Investigation, Methodology, Supervision, Writing – original draft, Writing – review & editing

    Affiliations School of Life Sciences, University of Technology Sydney, Sydney, NSW, Australia, Department of Watershed Sciences and Ecology Center, Utah State University, Logan, UT, United States of America

  • David J. Booth,

    Roles Funding acquisition, Supervision, Writing – review & editing

    Affiliation School of Life Sciences, University of Technology Sydney, Sydney, NSW, Australia

  • Elizabeth M. P. Madin,

    Roles Conceptualization, Investigation, Writing – review & editing

    Affiliations Department of Biological Sciences, Macquarie University, Sydney, NSW, Australia, Hawai’i Institute of Marine Biology, University of Hawai’i, Kane’ohe, HI, United States of America

  • Charles Hinchliffe,

    Roles Formal analysis, Writing – original draft, Writing – review & editing

    Affiliations School of Life Sciences, University of Technology Sydney, Sydney, NSW, Australia, School of Biological, Earth and Environmental Sciences, University of New South Wales, Sydney, NSW, Australia

  • Alastair R. Harborne,

    Roles Conceptualization, Investigation, Methodology, Writing – review & editing

    Affiliations Marine Spatial Ecology Laboratory and Australian Research Council Centre of Excellence for Coral Reef Studies, School of Biological Sciences, University of Queensland, Brisbane, QLD, Australia, Department of Biological Sciences, Florida International University, North Miami, Florida, United States of America

  • Catherine E. Lovelock,

    Roles Conceptualization, Funding acquisition, Writing – review & editing

    Affiliations Global Change Institute, University of Queensland, St. Lucia, QLD, Australia, School of Biological Sciences University of Queensland, St. Lucia, QLD, Australia

  • Peter I. Macreadie,

    Roles Resources, Validation, Writing – review & editing

    Affiliation Centre for Integrative Ecology, School of Life and Environmental Sciences, Faculty of Science Engineering and Built Environment, Deakin University, Melbourne, VIC, Australia

  • Trisha B. Atwood

    Roles Conceptualization, Data curation, Formal analysis, Investigation, Methodology, Supervision, Writing – original draft, Writing – review & editing

    Affiliations Department of Watershed Sciences and Ecology Center, Utah State University, Logan, UT, United States of America, Global Change Institute, University of Queensland, St. Lucia, QLD, Australia

Benthic meiofaunal community response to the cascading effects of herbivory within an algal halo system of the Great Barrier Reef

  • Quinn R. Ollivier, 
  • Edward Hammill, 
  • David J. Booth, 
  • Elizabeth M. P. Madin, 
  • Charles Hinchliffe, 
  • Alastair R. Harborne, 
  • Catherine E. Lovelock, 
  • Peter I. Macreadie, 
  • Trisha B. Atwood
PLOS
x

Abstract

Benthic fauna play a crucial role in organic matter decomposition and nutrient cycling at the sediment-water boundary in aquatic ecosystems. In terrestrial systems, grazing herbivores have been shown to influence below-ground communities through alterations to plant distribution and composition, however whether similar cascading effects occur in aquatic systems is unknown. Here, we assess the relationship between benthic invertebrates and above-ground fish grazing across the ‘grazing halos’ of Heron Island lagoon, Australia. Grazing halos, which occur around patch reefs globally, are caused by removal of seagrass or benthic macroalgae by herbivorous fish that results in distinct bands of unvegetated sediments surrounding patch reefs. We found that benthic algal canopy height significantly increased with distance from patch reef, and that algal canopy height was positively correlated with the abundances of only one invertebrate taxon (Nematoda). Both sediment carbon to nitrogen ratios (C:N) and mean sediment particle size (μm) demonstrated a positive correlation with Nematoda and Arthropoda (predominantly copepod) abundances, respectively. These positive correlations indicate that environmental conditions are a major contributor to benthic invertebrate community distribution, acting on benthic communities in conjunction with the cascading effects of above-ground algal grazing. These results suggest that benthic communities, and the ecosystem functions they perform in this system, may be less responsive to changes in above-ground herbivorous processes than those previously studied in terrestrial systems. Understanding how above-ground organisms, and processes, affect their benthic invertebrate counterparts can shed light on how changes in aquatic communities may affect ecosystem function in previously unknown ways.

Introduction

Above-ground ecosystem components and their benthic or below-ground counterparts are often studied in isolation of one another. However, the biota in these components are intricately connected through a series of complex interactions and processes [13]. For example, it is well known that soil and sediment communities are responsive to changes in the quality and quantity of organic matter entering their food web. These responses can manifest as shifts in the soil or sediment community composition, as well as alter the rate at which these communities perform essential ecosystem processes (e.g., decomposition) [4,5]. Conversely, soil and sediment communities break down dead organic matter, releasing the essential nutrients that fuel plant growth and influence plant diversity [68]. Thus, studies that explore the linkages between above-ground and benthic or epibenthic processes are essential for understanding the mechanisms that drive community and ecosystem dynamics.

In terrestrial ecosystems, the cascading effects of herbivore activities on below-ground community composition, transmitted through alterations to plant abundance and/or distributions, have been well documented [2,3,9,10]. These studies demonstrate that above-ground herbivores can alter the community composition of infaunal biota by changing the quantity and/or quality of resource inputs to soil communities, also likely influencing soil abiotic factors such as temperature and moisture [1]. These studies have also shown that herbivore-mediated changes to infauna have implications for nutrient cycling and other ecosystem functions that lead to feedbacks in the above-ground communities, highlighting some of the effects that anthropogenic changes to plant-herbivore systems (e.g., through invasive species or species extirpation) may have on the structure and functioning of terrestrial ecosystems. In contrast, investigations of trophic cascades in aquatic ecosystems have so far focused on infaunal herbivorous consumption of above- and below-ground biomass (e.g. crabs in tidal marshes) [11,12] or predator-prey interactions, and their indirect effects on primary producers [1315,11] and nutrient cycling [16], while little is currently known regarding the potential indirect effects of herbivory on benthic invertebrate communities [17].

One potential example of cascading effects being transmitted through grazing herbivores in aquatic ecosystems is that of marine ‘grazing halos’. Grazing halos, which occur around patch reefs globally, are caused by the removal of seagrass or macroalgae that results in a distinct band of unvegetated sediment surrounding a patch reef [1825]. Although the mechanisms behind the development of grazing halos are not fully understood, there is evidence that they develop as a result of differences in spatial patterns of herbivore foraging [22,24,25]. It is further hypothesized that this behaviour in herbivores reflects constraints imposed by predation risk, where herbivores reduce the spatial extent of their grazing to avoid unsheltered, high predation-risk areas further from patch reef refuges [19,26,27]. Regardless of the ultimate mechanism, this pattern of spatially constrained herbivore grazing results in zones of highly grazed sandy substrate close to patch reefs, and zones of elevated algal or seagrass biomass with increasing distance from the reef (Fig 1). This foraging behaviour by herbivores, and the resulting pattern in plant biomass, has the potential to influence benthic communities through several direct and indirect mechanisms similar to those of terrestrial systems, such as a reduction in primary producer food availability and therefore benthic invertebrate abundances [7,28], with flow on effects to secondary benthic consumers [29]. It is important to note that unlike terrestrial plants that maintain complex root and rhizome structures, aquatic macroalgal beds do not have true roots, thereby limiting their below-ground biomass, and potentially, their effects on benthic invertebrate populations. However, due to both the well understood reliance of benthic invertebrates on macroalgae as a food resource [3032], and the globally ubiquitous existence of these spatially structured herbivore grazing patterns in habitats with more complex root structures (e.g. seagrasses) [22,25,26,33], cascading effects of herbivores in grazing halo systems still have the potential to reach benthic invertebrates. To date no study has looked at how the development of these large-scale, commonly-occurring vegetation patterns affects the distribution and abundance of benthic invertebrate communities.

thumbnail
Fig 1. Effects of grazing on benthic algal distribution in a coral reef lagoon ecosystem.

A) Satellite image of algal halos within Heron Island lagoon. White lines indicate coral patch reefs; green lines indicate the approximate outer extent of bare sandy substrate (i.e., halos). B) Siganus doliatus, a small reef dwelling herbivore taking shelter in a tropical coral patch reef, at least partly as an anti-predator response. Although this particular species likely contributes little to halo formation beyond the reef due to its territorial ‘farming’ habits on the reef itself, the anti-predator sheltering behaviour it displays here is indicative of reef fishes in general. Predation risk is commonly cited as the ultimate mechanism leading to the spatially-constrained herbivore grazing patterns around coral patch reefs that lead to halo formation (photo: A. Harborne). C) Conceptual diagram illustrating how herbivore grazing patterns influence mean algal density and canopy height.

https://doi.org/10.1371/journal.pone.0193932.g001

To assess if and how the spatial distribution of above-ground grazing affects benthic communities in a ‘natural’ aquatic ecosystem unaffected by human activities (e.g. removal of top predators), we examined the distribution and community variation in sedimentary invertebrates in a series of well-studied algal grazing halos within the lagoon of Heron Island on Australia’s Great Barrier Reef (GBR). Heron Island’s lagoonal patch reefs represent an ideal location to study the effects of herbivory on benthic communities because satellite imagery has documented the occurrence of grazing halos in the algal beds surrounding these patch reefs in the lagoon dating back to at least 1999. Additionally, Madin et al. [22] found that algal consumption by herbivores significantly decreased with increasing distance from the patch reef concomitantly with algal canopy height increases, demonstrating that herbivory is likely a key mechanism underlying the occurrence of halos in this system.

To better understand the mechanisms behind benthic invertebrate patterns, we analysed the relationship between benthic invertebrate community composition and distance from patch reef edge. We then examined the potential drivers behind the observed patterns in the benthic communities. First, we investigated whether herbivore-mediated changes in algal canopy height with increasing distance from the reef edge explain benthic community composition. We then tested the alternative hypothesis that physicochemical processes (e.g. hydrodynamics, reef erosion, etc.), unrelated to grazing, could be influencing benthic communities. For this hypothesis we focused on sediment particle size as interstitial meiofauna’s diversity and composition is known to depend highly on sedimentary conditions [34]. We also investigated the effect of carbon to nitrogen ratios (C:N) in the sediment on benthic communities, because high productivity and high fish abundance on the patch reef could cause nutrient availability to be highest adjacent to the reef [35]. This pattern, if it occurred, would not be reflective of grazing patterns, but rather would reflect nutrients transported from the patch reef. Our study presents preliminary evidence of aquatic above-ground cascading effects indirectly affecting specific taxa of benthic invertebrate communities through algal grazing, discusses the mechanisms through which these effects may be transmitted, and highlights the areas of research required to further tease apart these dynamics.

Methods and materials

Study area and survey design

This study was conducted in the shallow waters (< 5 m) of Heron Island lagoon (23°27′S, 151°55′E) in the southern GBR. All sampling was conducted between November and December, 2014. Heron Island is part of the Capricorn-Bunker Group, a collection of 21 coral reefs within the Mackay / Capricorn Management Area of the GBR Marine Park. Between November–December Heron Island has an average maximum temperature of 28.5°C, an average minimum temperature of 22.8°C and an average rainfall of 72.05 mm [36]. Roughly half of Heron Island’s reefs are within a no-take area of the Marine National Park Zone, while the other half lie within a limited-use area of the Conservation Park Zone, subject to strict permit issue and limited forms of recreational fishing [37]. All patch reefs in this study lay within an area of ~0.81 km2, located within the former zone. Benthic invertebrate samples, sediment grain size, sediment nutrient samples, and algal surveys, were taken three hours prior to, and three hours after peak high tide. For direct comparison with previous work on Heron Island’s grazing halos, satellite imagery and GPS coordinates were used to select 14 patch reef sites that were the same as those of Madin et al. [22].

At each of the 14 patch reefs, a single transect was run from the reef edge to a distance of 30 metres. The longest diameter of each patch reef was of a similar size, averaging 17.8 ± 2.3 m. Transects were placed so as to leave the maximum distance between the end of each transect and any adjacent patch reefs (72.82 ± 18.28 m). A single invertebrate core sample, a single core sample for grain size and nutrients, and three individual algal surveys were taken at each of the six distances: 0 m (just off the reef), 3 m, 7.5 m, 15 m, 22 m and 30 m (Fig 1), roughly covering an equal area along both the inside and outside of the halos. This study was carried out in accordance with the Great Barrier Reef Marine Park Act (1975) and all protocol was approved by the Great Barrier Reef Marine Park Authority (Permit numbers: G14/37304.1 & G14/37182.1). No vertebrate fauna were taken or harmed, and no endangered or protected species were involved in this study.

Invertebrate collection and processing

Benthic invertebrates were sampled to 5 cm depth in the sediment using a 4 cm diameter corer. Surface invertebrates were not separated and as such both epibenthic and infaunal invertebrates are included in this study. Samples were preserved in sealed plastic bags with 40 ml of 70% ethyl alcohol to reduce organic matter decay. In the laboratory, benthic invertebrate sediment samples were rinsed through a 250 μm mesh sieve to separate finer particles, thereby decreasing the turbidity of the samples to facilitate increased detection of the organisms. For community abundance analyses all Polychaeta and Mollusca were classified to family level, while Nematoda and Arthropoda were identified to phylum. The diversity of each sample was calculated using the Shannon-Wiener Index [38] in conjunction with the lowest level of each taxon described above.

Environmental data collection and processing

The canopy height of benthic primary producers, comprising of only Enteromorpha spp. (synonimised now under genus Ulva), Cladophora spp. and Hincksia spp. (a small, fine brown algae), were recorded at each distance interval by using the average of three measurements taken in situ with callipers (± 1 mm error). At each site and distance a second sediment core (5 cm height, 4 cm diameter) was taken to measure mean particle size and for C:N analysis. Mean particle size was calculated using a Mastersizer particle size analyser (Malvern Instruments, Malvern United Kingdom); all samples underwent a two-minute sonication pre-treatment for increased accuracy of finer particulates [39]. C:N was measured using a Costech Elemental Analyzer at the University of Hawaii at Hilo’s Marine Analytical Laboratory.

Data analyses

Benthic community data matrices (Bray-Curtis) were square root transformed for increased homoscedasticity [40]. For multivariate analyses, algal canopy height and mean particle size were normalised using Z-score transformation to account for differences in sampling units [41]. To analyse benthic invertebrate community variation, a mixed-effects PERMANOVA was used with distance from reef and particle size included as fixed terms, and patch reef identity included as a random factor to account for the multiple samples taken along each transect. Permutations were set at 9999, and significant factors were identified through step-wise removal of nonsignificant terms. The PERMDISP (Permutational Analysis of Multivariate Dispersions) function was used to determine whether significant PERMANOVA p-values were a result of variance around or between means. Distance Based Linear Models (DISTLM) were then used to determine the contribution of environmental covariates algal canopy height and mean sediment particle size to the overall multivariate assemblage variation [42]. Similarity Percentages Analyses (SIMPER) using overall community abundances were used to highlight groups driving any dissimilarity between distances.

Following initial analyses of the whole data set, and based on SIMPER percent contribution, benthic invertebrate assemblages were divided into their corresponding taxa: Polychaeta, Nematoda, Mollusca and Arthropoda. Individual groups were then analysed against distance from reef, algal canopy height, mean particle size and C:N ratio using linear mixed-effects models (LME) from the “lme()” function within “nlme” package in R [43], with patch reef again treated as a random factor. Invertebrate abundance homogeneity of variance at each distance level was confirmed. A polynomial (quadratic) equation was applied to distance from patch reef to allow for curvilinear relationships. Due to co-linearity between distance from patch reef and algal canopy height, where a quadtratic distance term was found to be insignificant it was removed completely and linear models were re-run [44]. Variables that made significant contributions to taxa-specific patterns were identified through Akaike Information Criterion (AIC) and step-wise removal of nonsignificant terms. The “predictSE.lme()” function, within the “AICcmodavg” package was implemented to approximate 95% confidence intervals of model fixed effects using the delta method. Two core samples from separate patch reefs at distances 30 m and 22 m were not used in the analyses due to missing nutrient and sediment particle size data, respectively. Data were analysed using PRIMERv6 (Primer-E Ltd, Plymouth, UK), PERMANOVA+ (Permutational Multivariate Analysis of Variance) and R 3.1.0 [45].

Results

Environmental patterns

Algal canopy height had a significant positive relationship with distance from patch reef (LME, f (1,67) = 76.631, P < 0.001, Fig 2A), and as such, these variables were not used together as predictors of benthic abundances through LMEs, and instead the best predictor was selected through the use of AIC. In contrast, mean surface sediment particle size (μm) showed a significant linear decrease with distance away from patch reef (LME, f (1, 67) = 8.055, P = 0.006, Fig 2B). Sediment C:N did not significantly vary with distance from patch reef (LME, Polynomial fixed effects, P > 0.05, Fig 2C), and likewise were not found to be significantly associated with algal canopy height (LME, P > 0.05, Fig 2D).

thumbnail
Fig 2. Linear mixed-effects models showing environmental patterns in the grazing halos of Heron Island lagoon.

Patch reef is treated as a random factor within the model to account for between site dissimilarity. Benthic algal canopy is expressed as height (mm), * indicates significance. Solid line indicates the predicted LME model fit, and dashed lines represent 95% confidence interval; N patch reefs sampled = 14.

https://doi.org/10.1371/journal.pone.0193932.g002

Invertebrate communities

A total of 4832 benthic invertebrates were identified. Overall, benthic invertebrate community composition matrices consisted of 14 groups, made up by arthropods (42%), molluscs (1.6%), nematodes (31.2%), and 11 groups of polychaetes (25.2%), the latter identified down to the lowest taxonomic level possible (i.e. family or unknown). Arthropoda consisted predominantly of harpacticoid copepods while Mollusca of bivalves. Each of these taxa were recorded as the total abundance within the sediment sample, and the multivariate analyses used taxa abundances, rather than taxa presence/absence to quantify differences among communities. Benthic communities significantly varied with distance from patch reef edge (Pseudo-f (5, 65) = 1.489, P = 0.038). Pair-wise analyses (Student–Newman–Keuls) indicated significant community changes between distances 3–22 m (SNK, df, 13, t, 1.624, P = 0.022) and 3–30 m (SNK, df, 13, t, 1.664, P = 0.022), while all other comparisons between distances indicated multivariate community homogeneity (P > 0.05). However, marginal tests resulting from DISTLM analyses indicated that particle size (Pseudo-f = 1.078, P = 0.352) and algal canopy height (Pseudo-f = 1.368, P = 0.205) were not significant contributers to this overall community variation. A linear-mixed effects model was best fit to invertebrate diversity (Shannon-Weiner Index) with variables algal canopy height (LME, f (1, 66) = 0.268, P = 0.606) and C:N ratios (LME, f (1, 66) = 0.918, P = 0.342), showing no significant correlation with either variable.

Community composition data were found to have heterogeneous variances around group mean values (PERMDISP, f (5, 78) = 3.48, P = 0.023). This variation in dispersions may have inflated the risk of type I error in community analyses, however this study retained a well-balanced experimental design, enhancing the robustness of PERMANOVA towards heterogeneity [46]. Due to 51% of benthic invertebrate sampling cores containing no molluscs and the remaining samples averaging an abundance of 1.02 ± 0.1, the observed variations in Mollusca abundances were considered too weak to interpret further through linear mixed-effects models.

Taxa-specific patterns were analysed to investigate the differences in community composition with distance from the patch reef and the mechanisms behind these differences. SIMPER analysis showed the highest contributors to community dissimilarity were the abundances of Arthropoda (19.81 ± 0.48%) followed by Nematoda (14.23 ± 0.57%), and Family; Dorvilleidae (Polychaeta, 12.75 ± 0.39%), with the residual dissimilarity attributed to the remaining 12 groups of Polychaeta, and grouped Mollusca (< 10% contribution per group). Linear mixed-effects models, using grouped invertebrate abundances and AIC model selection, were used to highlight distribution patterns across grazing halos. Total invertebrate abundances were best modelled linearly with only distance from reef included, showing a nonsignificant relationship (LME, f (1, 67) = 1.794, P = 0.185). Polychaeta-specific abundance were non-significantly related to both algal canopy height (LME, f (1, 66) = 0.643, P = 0.4254) and mean sediment particle size (LME, f (1, 66) = 2.137, P = 0.149). Arthropoda abundances exhibited a significant positive relationship with mean sediment particle size (LME, f (1, 66) = 6.070, P = 0.0163, Fig 3A), but a nonsignificant relationship with algal canopy height (LME, f (1, 66) = 3.496, P = 0.066). In contrast, Nematoda abundances were found to be positively related to algal canopy height (LME, f (1, 66) = 5.149, P = 0.027, Fig 3C), though there was increased uncertainty in the model around higher canopy heights. In addition, Nematoda abundances were significantly greater where higher sediment C:N was present (LME, f (1, 66) = 10.330, P = 0.002, Fig 3B).

thumbnail
Fig 3. Linear mixed-effects models showing the relationships between grouped taxon abundances and environmental conditions in the grazing halos of Haron Island Lagoon.

Patch reef is treated as a random factor within the model to account for between site dissimilarity. * indicates significance in the model. Solid line indicates the predicted LME model fit, and dashed lines represent 95% confidence interval; N patch reefs sampled = 14.

https://doi.org/10.1371/journal.pone.0193932.g003

Discussion

In aquatic ecosystems, benthic community structure is fundamental to both carbon and nutrient cycling at the sediment-water interface [6,8,30,31,47]. Abiotic drivers of benthic communities have been extensively studied [4851], however little is known regarding the effects of above-ground biotic processes, and their possible cascading influence on benthic biota. This study of grazing halos in Heron Island lagoon demonstrates that the major factors influencing spatial differences in benthic invertebrates are taxon-dependent. While Nematoda responded significantly to both spatial differences in algal canopy height and sediment nutrient concentrations, Athropoda responded only to sediment particle size and Polychaeta was unaffected by any of our measured variables.

The only benthic taxon that showed a significant relationship with benthic algae was Nematoda, whose abundances were positively related to algal canopy height. This relationship between algae and Nematoda abundance is likely related to the fact that omnivorous nematodes, which have the ability to manipulate and digest large algal particles, have been shown to make up a large portion of the total Nematoda populations on the reef shelves and lagoons of the GBR [52]. In addition, marine nematodes are known to display spatial aggregations in their abundances [53], which have been suggested to be a result of selective consumption and settlement in optimal areas [5456]. For example, experiments by Ullberg and Ólafsson [56] demonstrated that Nematoda suspended in the water column are able to choose settling areas, displaying a clear preference for sediments with benthic algae, where their abundances were up to seven times higher than those of bare substrates.

In addition, several physicochemical properties of the sediments can also influence benthic communities. For example, variation in sediment particle size, largely attributed to physical weathering of coral structures and hydrological regimes [57,58], is widely accepted as a major driver of benthic invertebrate abundances in aquatic ecosystems [5962]. Sediment particle size shapes benthic biota by creating conditions in which optimal body sizes are required for both interstitial living and sediment reworking [59], while also affecting sediment water and nutrient concentration [63], pore water oxygen exchange, and redox environment [64]. All are fundamental to benthic community structure [65]. In accordance with our hypothesis and previous literature, mean sediment particle size exerted a positive influence on Arthropoda abundances (predominantly copepods).

Sediment nutrient content (C:N) displayed a taxon-specific positive relationship with benthic communities, specifically Nematoda abundances. One mechanism that can alter nutrient levels in surface sediments is fish faecal deposition and the transportation of nutrients from the reef [35,62,66]. As fish reduce their foraging distance, they simultaneously spend an increased amount of time closer to their patch reef refugia [67], potentially resulting in higher nutrient concentrations in these areas. Sediment carbon content not only affects the amount of easily broken down organic matter directly available for benthic invertebrate consumption, but also promotes differering communities of bacteria (C:N >30:1) and fungi (C:N <30:1), with flow on effects to bactivorous and fungivorous invertebrates [68]. However, C:N ratios in the sediments were not significantly related to distance from patch reef or algal canopy height. These results suggest that the drivers of sediment nutrient content, independent from fish faecal deposition and algal growth, also play a key role in shaping benthic invertebrate abundances in these systems.

Separate from the cascading effects of herbivores through primary producer distribution, and outside the scope of this study, are the consumptive effects of fish predation on benthic invertebrate abundances [13]. Invertivorous coral reef fish species are theoretically subject to the same behavioural pressures as those of their herbivorous neighbours, and as such would potentially exert direct effects on benthic invertebrate abundances along a distance from patch reef gradient. These direct effects would likely have a strong influence on the benthic invertebrate distributions analysed here. Under this scenario, distance from patch reef could be used as a proxy for invertivorous fish foraging. However, within this study linear mixed effects models on grouped invertebrate abundances, with AIC model selection including all covariates, indicated that distance from patch reef should be excluded for greater model fit (apart from total abundances that showed a nonsignificant relationship with distance). As such, we can assume that the relationships between algal canopy height and benthic invertebrates observed here are robust to predatory effects.

The primary goal of this study was to investigate potential cascading influences of above-ground aquatic grazing, through changes to benthic primary production, on benthic invertebrate communities. Our findings suggest that only Nematoda populations responded to differences in benthic algal canopy height indicating that although present, cascading effects of this type are a weak driver of benthic communities in this benthic algal dominated system. We also found that the observed cascading effects exert influence on benthic communities in conjunction with other well known environmental factors (i.e. sediment particle size and sediment C:N). These results suggest that in this system, benthic invertebrate communities and the ecosystem functions they perform, may be less responsive to changes in above-ground processes than those that have been studied in terrestrial systems. Further studies are needed to understand whether the observed benthic invertebrate community response to above-ground herbivory found in this study is ubiquitous across both temporal scales (i.e. fluctuations in algal biomass) and other marine vegetated ecosystems.

Supporting information

S1 File. Invertebrate abundances with distance away from patch coral reef.

Excel file that consists of algal canopy height (mm), grouped invertebrate abundances, mean sediment particle size (μm), carbon to nitrogen ratios (C:N) and diversity (Shannon-Weiner index) at each distance interval away from patch reef (m); 0, 3, 7.5, 15, 22 and 30.

https://doi.org/10.1371/journal.pone.0193932.s001

(XLSX)

Acknowledgments

This research was funded by a Global Change Institute Seed Grant to T.B.A, C.E.L., and A.R.H., Australian Research Council DECRA Fellowships to E.M.P.M. (DE120102614), A.R.H. (DE120102459), and P.I.M. (DE130101084), a World Wildlife Fund Kathryn S. Fuller Science for Nature Fund awarded to E.M.P.M., a US National Science Foundation International Postdoctoral Fellowship awarded to E.M.P.M, and The Marine and Coastal Carbon Biogeochemistry Cluster. We would like to thank B. Sullivan and E. Darling for help in the field and T. Holizski, T. Wiegner and the University of Hawaii at Hilo analytical lab for sample analyses. This is contribution #85 from the Center for Coastal Oceans Research in the Institute for Water and Environment at Florida International University.

References

  1. 1. Bardgett RD, Wardle DA. Herbivore‐mediated linkages between aboveground and belowground communities. Ecology 2003;84:2258–68.
  2. 2. Wardle DA, Bardgett RD, Klironomos JN, Setala H, van der Putten WH, Wall DH. Ecological linkages between aboveground and belowground biota. Science 2004;304:1629–33. pmid:15192218
  3. 3. Wardle D. Trophic cascades, aboveground and belowground linkages, and ecosystem functioning. Trophic Cascades Predat Prey Chang Dyn Nat 2010:203.
  4. 4. Hawlena D, Strickland MS, Bradford MA, Schmitz OJ. Fear of predation slows plant-litter decomposition. Science 2012;336:1434–8. pmid:22700928
  5. 5. Hinchliffe C, Atwood T, Ollivier Q, Hammill E. Presence of invasive Gambusia alters ecological communities and the functions they perform in lentic ecosystems. Mar Freshw Res 2017.
  6. 6. Norling K, Rosenberg R, Hulth S, Grémare A, Bonsdorff E. Importance of functional biodiversity and species-specific traits of benthic fauna for ecosystem functions in marine sediment. Mar Ecol Prog Ser 2007;332:11–23.
  7. 7. Kristensen E, Bouillon S, Dittmar T, Marchand C. Organic carbon dynamics in mangrove ecosystems: a review. Aquat Bot 2008;89:201–19.
  8. 8. Mermillod-Blondin F. The functional significance of bioturbation and biodeposition on biogeochemical processes at the water—sediment interface in freshwater and marine ecosystems. J North Am Benthol Soc 2011;30:770–8.
  9. 9. Van der Putten WH, Vet LEM, Harvey JA, Wackers FL. Linking above- and belowground multitrophic interactions of plants, herbivores, pathogens, and their antagonists. Trends Ecol Evol 2001;16:547–54.
  10. 10. Fukami T, Wardle DA, Bellingham PJ, Mulder CPH, Towns DR, Yeates GW, et al. Above- and below-ground impacts of introduced predators in seabird-dominated island ecosystems. Ecol Lett 2006;9:1299–307. pmid:17118004
  11. 11. Holdredge C, Bertness MD, Herrmann NC, Gedan KB. Fiddler crab control of cordgrass primary production in sandy sediments. Mar Ecol Prog Ser 2010;399:253–9.
  12. 12. Coverdale TC, Altieri AH, Bertness MD. Belowground herbivory increases vulnerability of New England salt marshes to die‐off. Ecology 2012;93:2085–94. pmid:23094380
  13. 13. Moksnes P, Gullström M, Tryman K, Baden S. Trophic cascades in a temperate seagrass community. Oikos 2008;117:763–77.
  14. 14. Lewis LS, Anderson TW. Top‐down control of epifauna by fishes enhances seagrass production. Ecology 2012;93:2746–57. pmid:23431604
  15. 15. Heithaus MR, Wirsing A, Dill L. The ecological importance of intact top-predator populations: a synthesis of 15 years of research in a seagrass ecosystem. Mar Freshw Res 2012;63:1039–50.
  16. 16. Atwood TB, Connolly RM, Ritchie EG, Lovelock CE, Heithaus MR, Hays GC, et al. Predators help protect carbon stocks in blue carbon ecosystems. Nat Clim Change 2015;5:1038–45.
  17. 17. Shurin JB, Borer ET, Seabloom EW, Anderson K, Blanchette CA, Broitman B, et al. A cross-ecosystem comparison of the strength of trophic cascades. Ecol Lett 2002;5:785–791.
  18. 18. Randall JE. Grazing effect on sea grasses by herbivorous reef fishes in the West Indies. Ecology 1965:255–60.
  19. 19. Ogden JC, Brown RA, Salesky N. Grazing by the echinoid Diadema antillarum Philippi: formation of halos around West Indian patch reefs. Science 1973;182:715–7. pmid:17817963
  20. 20. Sweatman H, Robertson DR. Grazing halos and predation on juvenile Caribbean surgeonfishes. Mar Ecol Prog Ser 1994:1–6.
  21. 21. Armitage AR, Fourqurean JW. The short-term influence of herbivory near patch reefs varies between seagrass species. J Exp Mar Biol Ecol 2006;339:65–74.
  22. 22. Madin EMP, Madin JS, Booth DJ. Landscape of fear visible from space. Sci Rep 2011;1. pmid:22355533
  23. 23. Burkholder DA, Heithaus MR, Fourqurean JW, Wirsing A, Dill LM. Patterns of top‐down control in a seagrass ecosystem: could a roving apex predator induce a behaviour‐mediated trophic cascade? J Anim Ecol 2013;82:1192–202. pmid:23730871
  24. 24. Downie RA, Babcock RC, Thomson DP, Vanderklift MA. Density of herbivorous fish and intensity of herbivory are influenced by proximity to coral reefs. Mar Ecol Prog Ser 2013;482:217–25.
  25. 25. Madin EM, Dill LM, Ridlon AD, Heithaus MR, Warner RR. Human activities change marine ecosystems by altering predation risk. Glob Change Biol 2016;22:44–60.
  26. 26. Ogden JC. Some aspects of herbivore-plant relationships on Caribbean reefs and seagrass beds. Aquat Bot 1976;2:103–16.
  27. 27. Ogden JC, Lobel PS. The role of herbivorous fishes and urchins in coral reef communities. Environ Biol Fishes 1978;3:49–63.
  28. 28. Kristensen E, Penha-Lopes G, Delefosse M, Valdemarsen T, Quintana C, Banta G. What is bioturbation? The need for a precise definition for fauna in aquatic sciences. Mar Ecol Prog Ser 2012;446:285–302.
  29. 29. Bardgett RD, Wardle DA, Yeates GW. Linking above-ground and below-ground interactions: how plant responses to foliar herbivory influence soil organisms. Soil Biol Biochem 1998;30:1867–78.
  30. 30. Nicotri M. Factors involved in herbivore food preference. J Exp Mar Biol Ecol 1980;42:13–26.
  31. 31. Cruz-Rivera E, Hay ME. Can quantity replace quality? Food choice, compensatory feeding, and fitness of marine mesograzers. Ecology 2000;81:201–19.
  32. 32. Ruitton S, Francour P, Boudouresque C. Relationships between algae, benthic herbivorous invertebrates and fishes in rocky sublittoral communities of a temperate sea (Mediterranean). Estuar Coast Shelf Sci 2000;50:217–30.
  33. 33. Ruiz-Reynés D, Gomila D, Sintes T, Hernández-García E, Marbà N, Duarte CM. Fairy circle landscapes under the sea. Sci Adv 2017;3:e1603262. pmid:28782035
  34. 34. Leduc D, Rowden AA, Probert PK, Pilditch CA, Nodder SD, Vanreusel A, et al. Further evidence for the effect of particle-size diversity on deep-sea benthic biodiversity. Deep Sea Res Part Oceanogr Res Pap 2012;63:164–9.
  35. 35. Burkepile DE, Allgeier JE, Shantz AA, Pritchard CE, Lemoine NP, Bhatti LH, et al. Nutrient supply from fishes facilitates macroalgae and suppresses corals in a Caribbean coral reef ecosystem. Sci Rep 2013;3:srep01493.
  36. 36. ABoM. Australian Bureau of Meteorology. Climate statistics for Australian locations (Heron Island). 2015. http://www.bom.gov.au/climate/averages/tables/cw_039122.shtml (accessed September 7, 2015).
  37. 37. GBRMPA. Great Barrier Reef Marine Park Authority, Marine Park Zoning, MAP 18—Capricorn Bunker Group 2011.
  38. 38. Molles MC, Cahill JF. Ecology: concepts and applications. WCB/McGraw-Hill Dubuque, IA; 1999.
  39. 39. Vdović N, Obhođaš J, Pikelj K. Revisiting the particle-size distribution of soils: comparison of different methods and sample pre-treatments. Eur J Soil Sci 2010;61:854–64.
  40. 40. Anderson M. PERMDISP: a FORTRAN computer program for permutational analysis of multivariate dispersions (for any two-factor ANOVA design) using permutation tests. Dep Stat Univ Auckl N Z 2004:24.
  41. 41. Jain A, Nandakumar K, Ross A. Score normalization in multimodal biometric systems. Pattern Recognit 2005;38:2270–85.
  42. 42. Anderson M. DISTLM v. 5: a FORTRAN computer program to calculate a distance-based multivariate analysis for a linear model. Dep Stat Univ Auckl N Z 2004;10.
  43. 43. Pinheiro J, Bates D, DebRoy S, Sarkar D, R Core Team. nlme: Linear and Nonlinear Mixed Effects Models. 2015.
  44. 44. Zuur AF, Ieno EN, Elphick CS. A protocol for data exploration to avoid common statistical problems. Methods Ecol Evol 2010;1:3–14.
  45. 45. R Core Team. R: A language and environment for statistical computing. R Foundation for Statistical Computing. Vienna, Austria: 2014.
  46. 46. Anderson M, Walsh DC. PERMANOVA, ANOSIM, and the Mantel test in the face of heterogeneous dispersions: What null hypothesis are you testing? Ecol Monogr 2013;83:557–574.
  47. 47. Aller RC. The importance of the diffusive permeability of animal burrow linings in determining marine sediment chemistry. J Mar Res 1983;41:299–322.
  48. 48. Statzner B, Higler B. Stream hydraulics as a major determinant of benthic invertebrate zonation patterns. Freshw Biol 1986;16:127–39.
  49. 49. Rodriguez SR, Ojeda FP, Inestrosa NC. Settlement of benthic marine invertebrates. Mar Ecol Prog Ser Oldendorf 1993;97:193–207.
  50. 50. Borja A, Franco J, Pérez V. A marine biotic index to establish the ecological quality of soft-bottom benthos within European estuarine and coastal environments. Mar Pollut Bull 2000;40:1100–14.
  51. 51. Von Bertrab MG, Krein A, Stendera S, Thielen F, Hering D. Is fine sediment deposition a main driver for the composition of benthic macroinvertebrate assemblages? Ecol Indic 2013;24:589–98.
  52. 52. Alongi D, Tietjen J. Population growth and trophic interactions among free-living marine nematodes. Popul Growth Trophic Interact Free-Living Mar Nematodes 1980:151–66.
  53. 53. Olafsson E. Do macrofauna structure meiofauna assemblages in marine soft-bottoms? A review of experimental studies. Vie Milieu-Life Environ 2003;53:249–65.
  54. 54. Lee J, Tietjen J, Mastropaolo C, Rubin H. Food quality and the heterogeneous spatial distribution of meiofauna. Helgoländer Wiss Meeresunters 1977;30:272.
  55. 55. Hogue E, Miller C. Effects of sediment microtopography on small-scale spatial distributions of meiobenthic nematodes. J Exp Mar Biol Ecol 1981;53:181–91.
  56. 56. Ullberg J, Ólafsson E. Free-living marine nematodes actively choose habitat when descending from the water column. Mar Ecol Prog Ser 2003;260:141–9.
  57. 57. Stoddart D, Steers J. The nature and origin of coral reef islands. Biol Geol Coral Reefs 1977;4:59–105.
  58. 58. Glynn PW, Manzello DP. Bioerosion and coral reef growth: a dynamic balance. Coral Reefs Anthr., Springer; 2015, p. 67–97.
  59. 59. Schwinghamer P. Characteristic size distributions of integral benthic communities. Can J Fish Aquat Sci 1981;38:1255–63.
  60. 60. Taghon GL. Optimal foraging by deposit-feeding invertebrates: roles of particle size and organic coating. Oecologia 1982;52:295–304. pmid:28310387
  61. 61. Duplisea DE, Drgas A. Sensitivity of a benthic, metazoan, biomass size spectrum to differences in sediment granulometry. Mar Ecol Prog Ser 1999:73–81.
  62. 62. Giere O. Meiobenthology: The Microscopic Motile Fauna of Aquatic Sediments. Springer Science & Business Media; 2008.
  63. 63. Williams R. The abundance and biomass of the interstitial fauna of a graded series of shell-gravels in relation to the available space. J Anim Ecol 1972:623–46.
  64. 64. Jansson B-O. The significance of grain size and pore water content for the interstitial fauna of sandy beaches. Oikos 1967:311–22.
  65. 65. Snelgrove P, Butman C. Animal-sediment relationships revisited: cause versus effect. Oceanogr Lit Rev 1995;8:668.
  66. 66. Coull BC. Are members of the meiofauna food for higher trophic levels? Trans Am Microsc Soc 1990:233–46.
  67. 67. Madin EM, Gaines SD, Madin JS, Warner RR. Fishing indirectly structures macroalgal assemblages by altering herbivore behavior. Am Nat 2010;176:785–801. pmid:20961223
  68. 68. Moore JC, Berlow EL, Coleman DC, Ruiter PC, Dong Q, Hastings A, et al. Detritus, trophic dynamics and biodiversity. Ecol Lett 2004;7:584–600.