Earthquake-driven destruction of an intertidal habitat cascade

Journal Pre-proof Earthquake-driven destruction of an intertidal habitat cascade Mads S. Thomsen, Isis Metcalfe, Alfonso Siciliano, Paul M. South, Shawn Gerrity, Tommaso Alestra, David R. Schiel

PII:

S0304-3770(20)30027-9

DOI:

https://doi.org/10.1016/j.aquabot.2020.103217

Reference:

AQBOT 103217

To appear in:

Aquatic Botany

Received Date:

16 August 2019

Revised Date:

4 February 2020

Accepted Date:

10 February 2020

Please cite this article as: Thomsen MS, Metcalfe I, Siciliano A, South PM, Gerrity S, Alestra T, Schiel DR, Earthquake-driven destruction of an intertidal habitat cascade, Aquatic Botany (2020), doi: https://doi.org/10.1016/j.aquabot.2020.103217

This is a PDF file of an article that has undergone enhancements after acceptance, such as the addition of a cover page and metadata, and formatting for readability, but it is not yet the definitive version of record. This version will undergo additional copyediting, typesetting and review before it is published in its final form, but we are providing this version to give early visibility of the article. Please note that, during the production process, errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain. © 2020 Published by Elsevier.

Earthquake-driven destruction of an intertidal habitat cascade

Mads S. Thomsen, Isis Metcalfe, Alfonso Siciliano, Paul M. South, Shawn Gerrity, Tommaso Alestra, David R. Schiel

Corresponding author: Mads Solgaard Thomsen, christchurch, NEW ZEALAND

Highlights 

Large-scale disturbances, including earthquakes and seismic uplifts, can swiftly kill

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On 14 November 2016, a 7.8 Mw earthquake uplifted intertidal reefs along 110 km on the Kaikōura, New Zealand coastline.

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Habitat-forming fucoid seaweeds and their associated invertebrates were greatly

Epiphytes associated with these seaweeds, especially Notheia anomala, became

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functionally extinct after the earthquake. 

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reduced in abundance on uplifted intertidal reefs. 

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intertidal habitat-forming seaweeds.

Natural recovery is expected to be slow because of low propagule supply and negative

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feed-back mechanisms.

Abstract

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Large scale disturbances associated with anthropogenic activities or natural disasters can destroy primary habitat-forming species like corals, seagrasses and seaweeds. However, little research has documented if and on how large-scale disturbances affect secondary habitat

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formers, such as epiphytes and small animals that depend on biogenic habitats. Here we quantified changes in the abundance of both primary and secondary habitat-forming seaweeds as well as seaweed-associated invertebrates before and after a 7.8 Mw earthquake

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that uplifted four intertidal reef platforms by 0.5-0.8 m on the Kaikōura coastline in New Zealand. We found that the dominant primary (Hormosira banksii and three Cystophora species) and secondary (obligate and facultative epiphytes) habitat-forming seaweeds were all decimated and that mobile seaweed-associated animals were significantly less abundant (per gram of seaweed biomass) after the earthquake. Importantly, epiphytes became functionally extinct after the earthquake, as less than 0.1% of the populations survived, whereas primary habitat formers survived in suitable microhabitats, like water 1

covered tide-pools and tidal channels. Based on these results we also discuss possible cascading ecosystem effects and future scenarios for natural recovery vs. active restoration that could speed up the recovery of habitat-forming species on degraded reefs.

Keywords: obligate and facultative epiphytes, natural disasters, canopy-forming species, facilitation cascade, Hormosira banksii

Introduction

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Primary habitat-forming organisms, such as mangroves, bivalves, seagrasses and seaweed are of fundamental ecological importance and control ecological functions, biogeochemical

cycles and biodiversity across a variety of marine ecosystems (Bruno and Bertness, 2001;

Stachowicz, 2001; Thomsen et al., 2010). For example, standing seaweed biomass affects biodiversity by providing habitat for epiphytes, invertebrates and fish (Tuya et al., 2009;

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Thornber et al., 2016; Ramus et al., 2017). Furthermore, seaweeds also affect biogeochemical cycling, for example through photosynthetic carbon fixation, and, following dislodgment and

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breakages, can subsidise new detrital communities in adjacent habitats such as seagrass beds, salt marshes, sandy beaches and deep off-shore waters (Vanderklift and Wernberg, 2008;

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Thomsen et al., 2009; De Bettignies et al., 2013; Krause-Jensen and Duarte, 2016; Pedersen et al., 2019). Recently, the habitat-cascade concept has highlighted that primary habitatforming organisms also promote sequential habitat formation that can increase biodiversity

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through the provision of more or novel niche space and supplies of food (Thomsen et al., 2018; Gribben et al., 2019). Such primary habitat-forming organisms have been decimated in many parts of the world by anthropogenic activities (Halpern et al., 2008) and, occasionally,

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natural mega-disturbances including earthquakes and volcanic activity (Bodin and Klinger, 1986; Castilla, 1988; Castilla and Oliva, 1990; Castilla et al., 2010; Williams et al., 2010;

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Schiel et al., 2019). However, the implications of the combined loss of both primary and sequential habitat formers following severe disturbances are poorly understood because most studies have only focused on losses of primary habitat formers (Halpern et al., 2008). Here, we address this research gap by quantifying the abundance of primary and secondary habitatforming organisms and their associated biodiversity before and after a natural megadisturbance.

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Primary marine habitat formers facilitate secondary habitat formers such as sponges, tunicates and seaweeds (Wahl, 1989; Thomsen et al., 2010; Gribben et al., 2019). These secondary habitat formers, sometimes referred to as secondary structural species (Huston, 1994), keystone structures (Tews et al., 2004), ecosystem engineers (Jones et al., 1994), or foundation species (Angelini et al., 2011; Thomsen et al., 2018), can be found attached to, entangled around, or embedded within stands of primary habitat-forming species (Thomsen et al., 2018). It is increasingly recognized that secondary habitat-forming species can be important modifiers of ecosystem functioning, biodiversity and biogeochemical fluxes, but only a few studies have detailed their ecology in the context of disturbance (Thomsen et al.,

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2010; Angelini et al., 2011; Thomsen et al., 2018). It is important to understand how large-scale destruction events affect aquatic primary

producers, biodiversity, and community structure for the purposes of mitigation, amelioration and restoration, especially in instances where areas of high ecological, cultural and

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commercial value are impacted (Halpern et al., 2007; Bellgrove et al., 2010; Campbell et al., 2014). The impacts of localized disturbances such as wave action (Ebeling et al., 1985; Reed

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et al., 2011; De Bettignies et al., 2013), smothering by sediment (Airoldi, 1998), and grazing (Valentine and Johnson, 2005; Ling et al., 2015) are well studied and can be important determinants of ecological community structure and function (Dayton, 1971; Short and

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Wyllie-Echeverria, 1996). By comparison, studying large-scale mega-disturbances such as earthquakes is more difficult because their occurrences are rare, unpredictable and often

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devastating, preventing time-structured experiments and access to sites and supplies. Building a framework to predict impacts on shallow coastal systems from mega-disturbances is further complicated because underpinning processes operate over very different spatio-temporal

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scales. For example, following instantaneous uplifts, smaller scale processes like herbivory, competition, light availability and desiccation stress are dramatically altered in concert with

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larger scale processes like limited propagule pressure and disrupted population connectivity, (Castilla and Oliva, 1990; Waters et al., 2013; Schiel et al., 2019), making it challenging to predict survival and recovery trajectories. Nevertheless, case studies that document ecological impacts from mega-disturbances will increase our collective knowledge about what types of organisms are particularly sensitive (or resilient) and whether micro-habitats can modify effects. Here, we assessed the impact of earthquake caused uplift on large canopy-forming intertidal seaweed and their associated invertebrate communities along a 110 km stretch of the 3

Kaikōura coastline in New Zealand. More specifically, we compared the abundance of four primary habitat-forming seaweed species and a suite of secondary habitat-forming epiphytes as well as their associated invertebrates before and immediately after the earthquake. The primary habitat-forming species were the canopy-forming fucoids Hormosira banksii, Cystophora torulosa, C. scalaris and C. retroflexa. Hormosira is a desiccation tolerant midshore alga of up to 30 cm in length that is composed of simple chains of multiple bead-like vesicles. Cystophora torulosa is a low shore species growing to >50 cm that is morphologically more complex than Hormosira in that it has multiple branches that support 4-cm-long branchlets. Cystophora scalaris and C. retroflexa are typically lower shore –

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subtidal species that have complex morphologies with many branches and shorter (~ 1 cm), congested branchlets arising from their main stems (Adams, 1994; Schiel and Hickford,

2001; Schiel, 2006; Schiel, 2011). The secondary habitat formers quantified in this study were all epiphytes on the fucoid algae and included Notheia anomala (an obligate fucoid

epiphyte on H. banksii), Ceramium spp., Polysiphonia spp., and the articulated coralline,

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Jania sphaeroramosa. These epiphytes have complex, highly branched morphologies and

high surface-volume ratios (Adams, 1994; Meltcalfe, 2016; Thomsen et al., 2016b). Finally,

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we quantified the mobile invertebrates that were associated with primary and secondary biogenic habitats and used these data to speculate on earthquake-related cascading ecosystem

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effects and discuss recovery scenarios, including whether restoration is needed, and whether it should include secondary habitat formers in order to better promote recovery (Bellgrove et al., 2010) (Lawler et al., 2006; Halpern et al., 2007; Campbell et al., 2014; Marzinelli et al.,

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Methods

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2016).

Study sites. This study was conducted on four large intertidal flat rocky platforms at Cape

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Campbell and Kaikōura peninsula along the east coast of the South Island of New Zealand (Fig. 1). These platforms were intersected by channels and scattered with shallow (< 50 cm) tide pools that were dominated by dense assemblages of canopy-forming seaweeds providing habitat for a variety of other seaweeds and small invertebrates (Lilley and Schiel, 2006; Schiel, 2006; Schiel, 2011; Schiel et al., 2016; Thomsen et al., 2016b). The tidal range was c. 2 m and the intertidal canopy-forming algae generally occupied a band between 0 – 1 m above mean low water (mlw). On November 14 2016 the Kaikōura coastal regions 4

experienced a 7.8 Mw earthquake that uplifted much of the 110 km coastline from Goose bay south of Kaikōura to Cape Campbell (Schiel et al., 2018). Most of the coastline experienced an uplift of 1-2 m, with a maximum of almost 6 m at certain locations. The four study platforms were, by comparison, only uplifted 0.5-0.8 m and are still inundated at high tide thereby flushing the tidepools and channels twice a day (Fig. 1) (Hollingsworth et al., 2017; Shi et al., 2017; Schiel et al., 2018).

Intertidal habitat-forming seaweeds. We quantified the abundance of primary habitat-

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forming fucoid seaweed hosts (Hormosira banksii, Cystophora torulosa, C. scalaris, and C. retroflexa) and their smaller, secondary habitat-forming epiphytes (Notheia anomala and various red algae) on two intertidal reefs at Cape Campbell and two at Kaikōura, before

(January-February 2015) and after (February-March 2017) the earthquake. Fucoid seaweeds included Hormosira banksii in the mid to upper intertidal zone (0.5 – 1 m above mlw) and C.

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torulosa and Hormosira in the lower intertidal zone (0 – 0.5 m above mlw) (Schiel, 2006; Schiel et al., 2016). When Hormosira and C. torulosa were found in the lower zone, they

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were often inhabited by the obligate epiphyte Notheia anomala (Thomsen et al., 2016b) and epiphytic red algae (e.g., Ceramium spp., Polysiphonia spp. and Jania sphaeroramosa),

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respectively. The tide pools and channels were often dominated by C. scalaris and C. retroflexa, sometimes inhabited by the same red algal epiphytes.

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At each reef platform, photographs (= samples) were taken within the tidal zones and channels where Hormosira and Cystophora are commonly found. A total of 2486 photos were taken, with a minimum of 162 and maximum of 483 photos per reef before (summer

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2015) or after (summer 2017) the earthquake (see Fig. 1 for details). Each photo was taken 90 cm from, and perpendicular to, the substrate with the same camera, covering 0.97 m2 of reef

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(± 0.06 m2 SD, N = 15). Photos were randomly distributed within this tidal zone on the platform and therefore included tidal channels and tide pools. The percent cover of seaweed hosts and their epiphytes (> 1 cm) were estimated from each photo. Previous research has shown that >90% of the local epiphyte biomass is attached to the upper part of the host fronds (Meltcalfe, 2016; Siciliano, 2018). This implies that the large majority of epiphytes can be detected from photos and that this rapid and spatially extensive sampling methodology only under-estimates epiphyte abundances by an ecologically insignificant fraction. Our objective was to document reef-wide effects of the earthquake on habitat-forming seaweeds, so we did 5

not stratify data according to small variations in elevation or the patchy intersecting channels and tide pools. Percent cover data were non-normal, had many zeros, and high variance heterogeneity and could not be transformed to fulfil parametric statistical assumptions. We therefore pooled data across reefs and regions to compare relative abundances of the six taxa first before and then after the earthquake using Kruskal-Wallis 1-way analysis of variance (ANOVA) on rank tests, followed by post hoc SNK tests on ranked sums. We also calculated the average percent survival for each seaweed taxa using each reef as a replicate population

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(N = 4).

Seaweed-associated invertebrates. Before the earthquake, we had collected invertebrates

associated with the dominant habitat-forming seaweeds both in the presence and absence of

their most common epiphytes (Notheia attached to Hormosira, red algal epiphytes, including Jania sphaeroramosa and Polysiphonia spp., attached to the three Cystophora species). A

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total of 466 seaweed fronds were collected from the four reefs by cutting 10-15 cm of the

apical frond of each plant (either with or without attached epiphytes) and placing it into a zip-

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lock bag to prevent the loss of mobile invertebrates (Thomsen et al., 2016b). All the Cystophora samples were collected from tide pools during summer 2015 whereas Hormosira

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samples were collected from both tide pools and the intertidal platforms in 2013, 2014 and 2015 across all seasons. After the earthquake, 111 fronds were collected in fall 2017 and summer 2018 using similar methods and from the same four reefs. Fewer fronds were

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collected after the earthquake than before to minimize ecological impact on the sparse remnant seaweed populations. Furthermore, after the earthquake very few canopy-forming seaweed hosts had any attached epiphytes and only in small amounts. The ‘after-earthquake-

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epiphyte’ treatment had therefore both low replication levels and low epiphyte biomass (see Fig. 4 legend for details about replication levels and collected seaweed biomass). In the

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laboratory, samples were rinsed in freshwater onto a 250 m sieve. Invertebrates were classified as crustaceans, molluscs, polychaetes or ‘others’ and counted under a dissecting microscope (40). The total biomass of the seaweed frond (with epiphytes when present) was weighted after oven-drying at 65 C. Invertebrate counts were standardized to gram dry weight of seaweed. Data were then pooled across reefs and regions because not all combination of seaweed species and epiphytes could be sampled at all four reefs (e.g., more Hormosira samples were collected from the lower intertidal zone at sites on the Kaikōura

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peninsula). Three-way permutational analyses of variance (PERMANOVA) were used to test for the effects of the earthquake (2 levels; before and after), canopy-forming host species (four levels; Hormosira, C. torulosa, C. retroflexa and C. scalaris) and the two epiphytes (2 levels; with and without epiphytes) for each of the four invertebrate taxa. Data transformation did not achieve homogeneous variances and treatments were unbalanced, so results should be interpreted with caution. We adjusted alpha to 0.01 and interpreted mean effect cautiously, acknowledging that significant effects may alternatively have been caused by heterogeneous variances (Underwood, 1997). However, because we were interested in evaluating the Uplift  Host  Epiphyte interactions, and assessing the relative importance of the three test factors

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(Levine and Hullet, 2002), we used a biased factorial PERMANOVA over non-parametric ranked ANOVA that does not address interaction terms or relative importance of factors.

Significant results for the host test factor and the Host  Uplift interaction were followed by

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post-hoc t-tests.

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Results

Intertidal habitat-forming seaweeds. There were significant differences in abundances

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among seaweed taxa prior to the earthquake (Kruskall-Wallis; 2 = 2407.8, df = 5, p < 0.0001). Across all reefs, Hormosira was most abundant (present in 841 photos with a mean cover of 36%, Fig. 2A), followed by Cystophora scalaris (315 counts; 9% cover),

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Cystophora torulosa and N. anomala (ranked together statistically by SNK tests; 231 counts; 4% and 321 counts; 1.4%, respectively), and finally Cystophora retroflexa and red epiphytes (also ranked together; 63 counts, 0.8% and 94 counts, 0.7%, respectively) (Fig. 2A-B). After

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the earthquake, abundances of seaweed taxa were significantly different (2 = 1185, df = 5, p < 0.0001) with H. banksii being the most abundant species (379 counts; 0.78%, Fig. 2C)

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followed by C. scalaris (167 counts, 4.03%). Note however that H. banksii actually had lower mean cover than C. scalaris, but, because it was observed in many more samples it was, in the non-parametric Kruskal Wallis test, found to be statistically more abundant than C. scalaris (Underwood, 1997). Finally, the four remaining seaweed taxa were all statistically similarly ‘rare’ after the earthquake; that is, all taxa were found in very low abundances and only in a few samples (C. torulosa = 26 counts, 0.02% cover; C. retroflexa = 14 counts, 0.10%; Notheia = 12 counts, 0.002%; red filamentous epiphytes = 2 counts, 0.001%) (Fig. 2C-D). 7

Analysis of the reef- and population-wide survival rates for the six seaweed taxa indicated that epiphytes were more severely affected than their hosts (Fig. 3). More specifically, only 0.08% of the Notheia anomala populations attached to Hormosira and 0.05% of the epiphytic reds attached to Cystophora hosts, survived. By comparison, the primary habitat-forming hosts found on the tidal platforms had intermediate survival rates; that is 2.1% of Hormosira populations and 0.2% of C. torulosa populations survived. Finally, the primary habitat formers that dominated in the tidal channels and tide pools before the earthquake, had the greatest population survival rates with 20.1% of C. retroflexa and 14.5% of C. scalaris

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surviving.

Seaweed-associated invertebrates. Seaweed fronds were dominated by crustaceans (57.3

per gDW), followed by molluscs (22,7; primarily gastropods) with fewer polychaetes (1.8) and other invertebrates (0.5; Fig. 4, densities calculated by pooling across all test factors).

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Statistical analysis of crustacean abundances showed a significant Uplift  Host interaction with more crustaceans inhabiting C. Scalaris (278.7 per gDW) and C. retroflexa (219.2)

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compared to C. torulosa (120.0) and fewer inhabiting Hormosira (19.9) before the uplift. By contrast, there were no effects of host species on the abundance of crustaceans after the

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earthquake. In addition, C. scalaris (279 before vs. 72 after) and C. retroflexa (219 vs. 49) were inhabited by significantly fewer invertebrates per gram of biomass after the uplift. We also found a significant Uplift  Host interaction for molluscs. Again, there were no effects of

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hosts after the uplift, whereas more molluscs inhabited C. retroflexa, C. torulosa and C. scalaris (64.7, 49.4 and 46.1 ind. per gDW, respectively) compared to Hormosira (11.5) before the uplift. We also found significantly more molluscs on Hormosira after (23.5)

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compared to before (11.5), the uplift, but with no before-after differences for the three Cystophora species. In addition, more molluscs inhabited co-occurring hosts and epiphytes

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(39.9) compared to host species alone (12.9). The analysis of polychaetes also showed a significant Uplift  Host interaction with more polychaetes inhabiting C. retroflexa (18.8 per gDW) than C. torulosa, C. scalaris (7.3 and 5.8, statistically grouped together) and Hormosira (0.16) before the uplift. After the uplift fewer polychaetes inhabited Hormosira (0.18) than the three Cystophora species (grouped statistically together, 2.2-4.5 ind. per gDW). Finally, we found no statistical effects on other invertebrates, but these taxa only represented a small fraction of the seaweed-associated invertebrates.

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Discussion The uplift of reefs along the Kaikōura coastline in New Zealand had a devastating impact on intertidal primary and secondary habitat-forming seaweeds and on the mobile invertebrates that depend on these biogenic habitats. We expect there will be wider implications associated with this loss such as reduced primary production, habitat for juveniles of coastal species, organic cross-system subsidies and lost secondary production with potential ramifications for rock lobsters and fish of commercial, cultural and customary value (Choat, 1982; Edgar,

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1990b, a; Schiel, 2006; Wernberg et al., 2006; Schiel and Lilley, 2007; Thomsen et al., 2010; Tuya et al., 2010; Schiel et al., 2018).

Loss of primary habitat-forming hosts. The reefs at Cape Campbell and Kaikōura

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experienced a dramatic loss of primary habitat-forming seaweeds on large intertidal reefs following the c. 0.5-0.8 m uplift. This result was not surprising; intertidal seaweeds are

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marine organisms that typically are limited upwards by desiccation stress (Hatton, 1932; Schonbeck and Norton, 1979; Dromgoole, 1980; Brown, 1987). The hypothesis that

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increased desiccation stress caused the loss of canopy-forming seaweeds was supported by our population-survival results; species dominating the flat platforms (Hormosira, C. torulosa) had lower survival than species inhabiting tide pools and channels (C. scalaris, C.

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retroflexa) (Morton and Miller, 1973; Schiel, 2006; Schiel and Lilley, 2007; Schiel, 2011), some of which were still filled with water, after the uplift.

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Cystophora scalaris and C. retroflexa are common canopy-forming species in the shallow subtidal zone (Schiel and Hickford, 2001; Shears and Babcock, 2004) and the enhanced

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survival in tide pools suggests that subtidal populations could have also survived the uplift. However, because Hormosira and C. torulosa were rare in the former subtidal zone, these species have likely experienced more dramatic region-wide losses, and, depending on the extent and configuration of the new uplifted intertidal zone, may have slow recovery and only establish much smaller populations that therefore could be more susceptible to future stressors and local extinctions (Shaffer, 1981; Frankham, 1996).

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Loss of secondary habitat-forming epiphytes. Dramatic losses of primary habitat-forming species are visually striking and have been documented following large disturbances in previous studies (Castilla, 1988; Castilla and Oliva, 1990). However, it is more difficult to document the loss of less common and inconspicuous species such as epiphytes that can play an important ecological role through secondary habitat formation (Thomsen et al., 2018). This possibly explains why losses of marine epiphytes have not been documented following large scale disturbances – in contrast to recognized importance of terrestrial epiphytes in conservation ecology (Lõhmus and Lõhmus, 2010; Ellis et al., 2011). In this study, finely branched epiphytes with high surface-volume ratios provided important

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habitat for invertebrates, despite their low biomass (Fig. 4). This result was most striking for the morphologically simple Hormosira and relatively coarsely branched C. torulosa (with lowest surface-volume ratios) that provide poorer biogenic habitat compared to the more

complex C. scalaris and C. retroflexa (with intermediate surface-volume ratios). In other

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words, finely branched epiphytes enhanced the capacity of coarsely branched intertidal

seaweeds to provide habitat for small invertebrates. However, the finely branched structure of

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the epiphytes is likely also responsible for their poor resilience to uplift, because high surface-volume ratios cause high desiccation rates (Dromgoole, 1980; Thomsen et al., 2016b). At our study sites, the common red alga, Jania sphaeroramosa, Polysiphonia spp.,

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Ceramium spp. and Lophothamnion hirtum, are facultative epiphytes that can attach to a wide variety of hosts and rocky substrates (Adams, 1994). Therefore, there should be greater

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potential for red algal epiphytes to be resilient over large scales, because populations are likely to have survived in the subtidal zone. By contrast, Notheia is an obligate epiphyte that only attaches to Hormosira (Parrish, 1977; Thomsen et al., 2016b).

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The near extinction of Notheia on uplifted intertidal reefs suggests a long-term threat for this species; First, Notheia was disproportionally affected with only a few individuals surviving

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on the reefs. Second, Notheia is confined to a narrow elevation band and is susceptible to desiccation (Meltcalfe, 2016; Thomsen et al., 2016b). Third, the host Hormosira (and therefore also Notheia) is rare in the subtidal zone providing limited source populations to support recolonization. Finally, Notheia appears to be disproportionally more abundant on reefs with large Hormosira populations (Thomsen, pers. obs) and the new topography along uplifted coastline may not be suitable for the establishment of large Hormosira populations (Schiel et al., 2018). Taken in concert, this secondary habitat-forming species will likely occur in much lower abundances in the future (indeed, recent visits to the same impacted 10

reefs in November 2018 suggest even smaller populations of Notheia on surviving Hormosira hosts).

Loss of seaweed-associated invertebrates. The seaweeds sampled provided habitat for small mobile invertebrates, predominantly crustaceans and molluscs, as shown in other studies (Taylor and Cole, 1994; Taylor, 1997). More invertebrates generally inhabited the finer branched C. retroflexa and C. scalaris than the coarser branched Hormosira and C. torulosa (Russo, 1990; Taylor and Cole, 1994; Siciliano, 2018). This result could also reflect

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differences in micro-habitats between the primary habitat formers because fine-branched seaweeds were more common in the tide-pools and channels that might have been favourable to greater invertebrate survival. By comparison, the coarsely branched species were more

common on the intertidal platforms where desiccation stress can be strong (Lilley and Schiel, 2006; Meltcalfe, 2016; Thomsen et al., 2016b). Epiphytic facilitation of invertebrates was

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strongest for molluscs, a group that was dominated by herbivorous gastropods, when the

epiphytes were attached to coarsely branched hosts, supporting data from many other studies

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(Norton and Benson, 1983; Edgar and Robertson, 1992; Martin-Smith, 1993; Gartner et al., 2013; Thomsen et al., 2016b). Increased numbers of molluscs on epiphytes supports the

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‘affinity-distinctiveness’ hypothesis that predicts that habitat cascades should be strongest when inhabitants have affinity for secondary habitat formers that are form-functionally distinct from primary habitat formers (Thomsen et al., 2016a). In other words, grazing snails

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are particularly facilitated by finely branched palatable epiphytes attached to coarsely branched less palatable hosts. By contrast epiphytes attached to the morphologically more complex C. scalaris and C. retroflexa, only facilitated invertebrates by providing additional

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but functionally similar habitat space.

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In addition to the loss of animals, there are likely also cascading loss of secondary production and trophic provisioning along the uplifted coastline. We showed that more than 300 invertebrates inhabit each gram of seaweed (dry weight) on semi-protected intertidal reefs dominated by canopy-forming seaweeds. Scaling these results up to entire reefs suggest that billions of invertebrates were lost very quickly. However, these small mobile invertebrates typically have low habitat-affinities (Bell, 1991; Duffy and Hay, 1991; Taylor and Cole, 1994; Taylor, 1998) and conspecific taxa are likely to have survived the earthquake by inhabiting subtidal seaweeds, providing source populations for recolonization. Unfortunately, 11

little is known about the taxonomic identities, host affinities and niche breadth of small seaweed-associated invertebrates. It is possible that a few species have high host-specificity (e.g., for Hormosira or Notheia) and may therefore have been detrimentally affected by the loss of their hosts. Finally, we note that these animals provide a key trophic link to higher trophic levels, as an abundant food source for predatory fish, crabs, and rock lobster (Pinkerton et al., 2008; Feary et al., 2009).

Data limitations. Analyses of impacts following unpredictable disasters are typically limited

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by the availability of pre-disaster data as well as difficulties associated with reaching impacted sites and finding surviving organisms. Ideally, impact analyses are based on wellplanned Beyond-BACI designs (Benedetti-Cecchi, 2001), but it was clearly impossible to

anticipate this earthquake and uplift (Castilla, 1988; Castilla et al., 2010). Therefore, we had not collated data to fit the requirements of the Beyond-BACI analytical approach and we only

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have spatially extensive seaweed cover data for entire reefs from one survey prior to the

earthquake. However, these intertidal Hormosira-Cystophora seaweed communities have

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been present for at least 30 years when seaweed research was initiated along this coastline (Schiel, 2011; Schiel et al., 2016). Furthermore, our results are not representative of more

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exposed coastlines because Hormosira is not biomechanically adapted to strong wave action (Thomsen and Wernberg, 2005; McKenzie and Bellgrove, 2009). We also lacked an unimpacted ‘control’ site, but research from nearby regions (Banks peninsula, Moeraki

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peninsula) has shown no major changes to intertidal seaweed populations or seaweedassociated animals. A final discussion point is that seaweed cover was quantified from geotagged photos, a method that provides spatial references, allows suspicious data points to be

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revisited and corrected, and can be used to collect large amounts of data points in a short time frame (Foster et al., 1991; Dethier et al., 1993; Drummond and Connell, 2005; Abdo et al.,

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2006). In this study, data collection efficiency was of highest priority because the intertidal study sites were semi-remote reefs where seismic aftershocks and breakdown of infrastructure posed a significant threat (Hollingsworth et al., 2017; Shi et al., 2017; Schiel et al., 2018). It is well established that cover estimations from photos are accurate for large conspicuous and distinct species, such as the four canopy-forming hosts studied here (Foster et al., 1991; Dethier et al., 1993; Drummond and Connell, 2005; Abdo et al., 2006). Photos can also be used to quantify marine epiphytes, although abundances can be slightly underestimated if microscopic fragments and epiphytes attached to below-canopy stems are 12

overlooked (Miller-Myers and Virnstein, 1999; Virnstein, 1999; Borg et al., 2006). However, for our study species, most of the epiphytic biomass are found on upper parts of the host fronds and are visible from the photographs (Meltcalfe, 2016; Siciliano, 2018). Thus, preearthquake epiphyte abundances may be slightly under-estimated. However, after the earthquake only small and scattered host individuals survived, thereby eliminating ‘hidden’ sub-canopy epiphyte components. This implies that we may have slightly over-estimated epiphyte survival rates, but this bias only strengthens our conclusion that epiphytes were most severely affected. In other words, despite any of the discussed data limitations, our results clearly documented dramatic short-term losses of seaweed hosts and seaweed-associated

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invertebrates with particular severe losses of epiphytes.

Seaweed recovery and mitigation. The most important factor to determine the future

distribution of seaweed and associated invertebrates along the uplifted coastline is the new

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configuration of rocky reefs; specifically, whether there are now more or less intertidal and subtidal rocky reef space than before the earthquake. Our observations suggest that the

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Kaikōura coastline today has fewer, smaller and steeper wave protected intertidal reefs than before the earthquake (Schiel et al., 2018). As a result, this region will likely support fewer

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and smaller populations of Hormosira, Notheia and C. torulosa in the future. Another issue facing the Kaikōura coastline is accelerated erosion of newly uplifted rock, and the subsequent enhanced sediment deposition in the intertidal zone (Schiel et al., 2018; Schiel et

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al., 2019), resulting in either bare (and continually eroding) rock or gravel substrates at possible colonisation sites. Elsewhere along the uplifted coast, small green ephemeral seaweeds (Ulva spp.) have become abundant in lower to mid zones (Schiel et al., 2018;

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Schiel et al., 2019) and these seaweeds may compete for space with recolonizing primary

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habitat formers, at least in the short term (Sousa, 1979). Reductions in the quantity of subtidal reef could alter biotic forces (predation, grazing) that can be important in structuring intertidal communities, especially in the lower shore (Rilov and Schiel, 2006). To be successful, colonizers of the new intertidal zones of the uplifted reef must be able to tolerate the modified desiccation, light, temperature, sediment and hydrodynamics regimes. Furthermore, colonization is likely to be limited by propagule supply (Verling et al., 2005), genetic bottlenecks (Peery et al., 2012), allee-effects (Levitan and McGovern, 2005), competitors (Worm and Chapman, 1998) and grazers (Jenkins et al., 13

1999). For example, propagule pressure is now dramatically reduced. In addition, isolated and patchy new recruits of canopy-forming seaweed may be selectively targeted by grazers (Choat, 1982; Taylor and Schiel, 2010) or outcompeted by early colonizing opportunistic algae (Taylor and Schiel, 2003; Taylor et al., 2010; Alestra and Schiel, 2014; Alestra et al., 2014). It is therefore possible that reductions in suitable reef area and negative biotic feedback mechanisms could prevent colonization by canopy-forming fucoid seaweed over greater time scales. Indeed, in both eastern and Western Australia, canopy-forming seaweeds and their associated biodiversity have not recovered following large scale regional losses (Wernberg et al., 2013; Marzinelli et al., 2014; Marzinelli et al., 2016; Wernberg et al., 2016).

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If natural recolonization does not occur over the next few years, perhaps lost seaweed could

be rehabilitated to protect local biodiversity, food networks and recreational and commercial fisheries – as has been achieved in Australia (Bellgrove et al., 2010; Marzinelli et al., 2014). For example, seaweeds have been transplanted to suitable reef areas by seeding zygotes onto

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plates, ropes or the reef itself and by transplanting fertile individuals from other locations to

facilitate “natural” recruitment (Taylor and Schiel, 2003; Schiel et al., 2006; Bellgrove et al.,

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2010; Marzinelli et al., 2014). We suggest that it would also be beneficial to incorporate epiphytes in possible restoration projects. For example, transplanting Hormosira with attached epiphytic Notheia could better facilitate the recovery of this obligate epiphyte and its

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habitat cascade (Thomsen et al., 2016b). Similarly, opportunistic green algae (Ulva spp.) that now occupy much of the uplifted coastline (Schiel et al., 2018) may prevent colonization of

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the larger canopy-forming seaweed by pre-emption of space and sediment accumulation feedback mechanisms (Hay, 1981; Schiel et al., 2006; Alestra and Schiel, 2014; Alestra et al., 2014; Connell et al., 2014). Such enemy interactions could be reduced by removing

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competitors to maximize the survival of transplants and new propagules thereby speeding up the recovery of seaweeds. Using a combination of restoration methods may thereby support

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populations to exceed minimal viable population size thresholds and facilitate self-sustaining populations. Finally, we also suggest that restoration efforts are carried out in a population genetic context to preserve the original genetic diversity of surviving populations as much as possible (Lande, 1988; Fraser et al., 2009; Coleman et al., 2011; Bellgrove et al., 2016).

Author contributions

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Mads S. Thomsen conceptualized the paper, collected many data, analysed the data and wrote the paper. Paul M. South, Isis Metcalfe, Alfonso Siciliano, Shawn Gerrity, Tommaso Alestra, and David R. Schiel collected some of the data and commented on the various manuscripts draft versions.

Acknowledgements The authors greatly acknowledge their respective funding agencies: MST was funded by the Marsden Fund; PMS was funded by New Zealand Ministry of Business, Innovation and Employment under Contracts CAWX1315 and CAWX1801. Finally, we thank the Ministry of Business, Innovation, and Employment for the funding of recovery work (Recovery

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trajectories of the coastal marine ecosystem from the Kaikoura earthquakes).

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References

Jo

ur

na

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re

-p

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Abdo, D., Seager, J., Harvey, E., McDonald, J., Kendrick, G., Shortis, M., 2006. Efficiently measuring complex sessile epibenthic organisms using a novel photogrammetric technique. Journal of Experimental Marine Biology and Ecology 339, 120-133. Adams, N.M., 1994, Seaweeds of New Zealand. Canterbury University Press, 409 pps. Airoldi, L., 1998. Roles of disturbance, sediment stress, and substratum retention on spatial dominance in algal turf. Ecology 79, 2759-2770. Alestra, T., Schiel, D., 2014. Effects of opportunistic algae on the early life history of a habitatforming fucoid: influence of temperature, nutrient enrichment and grazing pressure. Marine Ecology Progress Series 508, 105-115. Alestra, T., Tait, L., Schiel, D., 2014. Effects of algal turfs and sediment accumulation on replenishment and primary productivity of fucoid assemblages. Marine Ecology Progress Series 511, 59-70. Angelini, C., Altieri, A.H., Silliman, B.R., Bertness, M.D., 2011. Interactions among foundation species and their consequences for community organization, biodiversity, and conservation. BioScience 61, 782-789. Bell, S.S., 1991. Amphipods as insect equivalents? An alternative view. Ecology 72, 350-354. Bellgrove, A., McKenzie, P.F., McKenzie, J.L., Sfiligoj, B.J., 2010. Restoration of the habitat-forming fucoid alga Hormosira banksii at effluent-affected sites: competitive exclusion by coralline turfs. Marine Ecology Progress Series 419, 47-56. Bellgrove, A., Rooyen, A., Weeks, A.R., Clark, J.S., Doblin, M.A., Miller, A.D., 2016. New resource for population genetics studies on the Australasian intertidal brown alga, Hormosira banksii: isolation and characterization of 15 polymorphic microsatellite loci through next generation DNA sequencing. Journal of Applied Phycology 3, 1721-1727. Benedetti-Cecchi, L., 2001. Beyond baci: optimatization of environmental sampling designs through monitoring and simulation. Ecological Applications 11, 783-799. Bodin, P., Klinger, T., 1986. Coastal uplift and mortality of intertidal organisms caused by the September 1985 Mexico earthquakes. Science 233, 1071-1074. Borg, J.A., Micallef, M.A., Schembri, P.J., 2006. Spatio‐temporal variation in the structure of a deep water Posidonia oceanica meadow assessed using non‐destructive techniques. Marine Ecology 27, 320-327. Brown, M.T., 1987. Effects of desiccation on photosynthesis of intertidal algae from a southern New Zealand shore. Botanica Marina 30, 121-127. Bruno, J.F., Bertness, M.D., 2001. Habitat modification and facilitation in benthic marine communities. Marine Community Ecology (Bertness, M.D., Gaines, S.D., Hay, M.E). Sinauer Associates, Inc., Sunderland, Massachusetts, 201-218. Campbell, A.H., Marzinelli, E.M., Vergés, A., Coleman, M.A., Steinberg, P.D., 2014. Towards restoration of missing underwater forests. PloS one 9. Castilla, J., Oliva, D., 1990. Ecological consequences of coseismic uplift on the intertidal kelp belts of Lessonia nigrescens in central Chile. Estuarine, Coastal and Shelf Science 31, 45-56. Castilla, J.C., 1988. Earthquake-caused coastal uplift and its effects on rocky intertidal kelp communities. Science 242, 440-443. Castilla, J.C., Manríquez, P.H., Camaño, A., 2010. Effects of rocky shore coseismic uplift and the 2010 Chilean mega-earthquake on intertidal biomarker species. Marine Ecology Progress Series 418, 1723. Choat, J.H., 1982. Fish feeding and the structure of benthic communities in temperate waters. Annual Review of Ecology and Systematics 13, 423-449.

16

Jo

ur

na

lP

re

-p

ro of

Coleman, M.A., Chambers, J., Knott, N.A., Malcolm, H.A., Harasti, D., Jordan, A., Kelaher, B.P., 2011. Connectivity within and among a network of temperate marine reserves. Plos One 6, e20168. Connell, S., Foster, M., Airoldi, L., 2014. What are algal turfs? Towards a better description of turfs. Marine Ecology Progress Series 495, 299-307. Dayton, P.K., 1971. Competition, disturbance, and community organization: the provision and subsequent utilization of space in a rocky intertidal community. Ecological Monographs 41, 351-389. De Bettignies, T., Wernberg, T., Lavery, P.S., Vanderklift, M.A., Mohring, M.B., 2013. Contrasting mechanisms of dislodgement and erosion contribute to production of kelp detritus. Limnology and Oceanography 58, 1680-1688. Dethier, M.N., Graham, E.S., Cohen, S., Tear, L.M., 1993. Visual versus random-point percent cover estimations:'objective'is not always better. Marine ecology progress series, 93-100. Dromgoole, F.I., 1980. Desiccation resistance of intertidal and subtidal algae. Botanica Marina 23, 149-159. Drummond, S.P., Connell, S.D., 2005. Quantifying percentage cover of subtidal organisms on rocky coasts: a comparison of the costs and benefits of standard methods. Marine and Freshwater Research 56, 865-876. Duffy, J.E., Hay, M.E., 1991. Amphipods are not all created equal: a reply to Bell. Ecology 72, 354358. Ebeling, A., Laur, D., Rowley, R.J.M.b., 1985. Severe storm disturbances and reversal of community structure in a southern California kelp forest. 84, 287-294. Edgar, G.J., 1990a. Predator-prey interactions in seagrass beds. I. The influence of macrofaunal abundance and size-structure on the diet and growth of the western rock lobster Panulirus cygnus George. Journal of Experimental Marine Biology and Ecology 139, 1-22. Edgar, G.J., 1990b. Predator-prey interactions in seagrass beds. III. Impacts of the western rock lobster Panulirus cygnus George on epifaunal gastropod populations. Journal of Experimental Marine Biology and Ecology 139, 33-42. Edgar, G.J., Robertson, A.I., 1992. The influence of seagrass structure on the distribution and abundance of mobile epifauna: pattern and processes in a Western Australian Amphibolis bed. Journal of Experimental Marine Biology and Ecology 160, 13-31. Ellis, C.J., Yahr, R., Coppins, B.J., 2011. Archaeobotanical evidence for a massive loss of epiphyte species richness during industrialization in southern England. Proceedings of the Royal Society of London B: Biological Sciences, rspb20110063. Feary, D.A., Wellenreuther, M., Clements, K., 2009. Trophic ecology of New Zealand triplefin fishes (family Tripterygiidae). Marine biology 156, 1703-1714. Foster, M.S., Harrold, C., Hardin, D.D., 1991. Point vs. photo quadrat estimates of the cover of sessile marine organisms. Journal of Experimental Marine Biology and Ecology 146, 193-203. Frankham, R., 1996. Relationship of genetic variation to population size in wildlife. Conservation Biology 10, 1500-1508. Fraser, C.I., Hay, C.H., Spencer, H.G., Waters, J.M., 2009. Genetic and morphological analyses of the southern bull kelp Durvillaea antartica (Phaeophycea: Durvillaeales) in New Zealand reveal cryptic species. Journal of Phycology 45, 436-443. Gartner, A., Tuya, F., Lavery, P.S., McMahon, K., 2013. Habitat preferences of macroinvertebrate fauna among seagrasses with varying structural forms. Journal of Experimental Marine Biology and Ecology 439, 143-151. Gribben, P.E., Angelini, C., Altieri, A.H., Bishop, M.J., Thomsen, M.S., Bulleri, F., 2019. Facilitation Cascades in Marine Ecosystems: A Synthesis and Future Directions. Oceanography and Marine Biology: An Annual Review 57, 127–216. Halpern, B.S., Silliman, B.R., Olden, J., Bruno, J., Bertness, M.D., 2007. Incorporating positive interactions in aquatic restoration and conservation. Frontiers in Ecology and the Environment 5, 153–160.

17

Jo

ur

na

lP

re

-p

ro of

Halpern, B.S., Walbridge, S., Selkoe, K.A., Kappel, C.V., Micheli, F., Agrosa, C., 2008. A global map of human impact on marine ecosystems. Science 319, 948–952. Hatton, H., 1932. Quelques observations sur le repeuplement en Fucus vesiculosus des surfaces rocheuses dénudées. Bulletin du Laboratoire de St-Servan 9, 1-6. Hay, M.E., 1981. The functional morphology of turf-forming seaweeds: persistence in stressful marine habitats. Ecology 62, 739-750. Hollingsworth, J., Ye, L., Avouac, J.P., 2017. Dynamically triggered slip on a splay fault in the Mw 7.8, 2016 Kaikoura (New Zealand) earthquake. Geophysical Research Letters 44, 3517-3525. Huston, M.A., 1994. Biological diversity: the coexistence of species on changing landscapes. Cambridge University Press, 681. Jenkins, S.R., Hawkins, S.J., Norton, T.A., 1999. Direct and indirect effects of a macroalgal canopy and limpet grazing in structuring a sheltered inter-tidal community. Marine Ecology Progress Series 188, 81-92. Jones, C.G., Lawton, J.H., Shachak, M., 1994. Organisms as ecosystem engineers. Oikos 69, 373-386. Krause-Jensen, D., Duarte, C.M., 2016. Substantial role of macroalgae in marine carbon sequestration. Nature Geoscience 9, 737-742. Lande, R., 1988. Genetics and demography in biological conservation. Science 241, 1455-1460. Lawler, J.J., Aukema, J.E., Grant, J.B., Halpern, B.S., Kareiva, P., Nelson, C.R., Ohleth, K., Olden, J.D., Schlaepfer, M.A., Silliman, B.R., Zaradic, P., 2006. Conservation science: a 20-year report card. Frontiers in Ecology and Environment 4, 473–480. Levine, T.R., Hullet, C.R., 2002. Eta squared, partial eta squared, and misreporting of effect size in communication research. Human Communication Research 28, 612-625. Levitan, D.R., McGovern, T.M., 2005. The Allee effect in the sea. Marine conservation biology: the science of maintaining the sea’s biodiversity. Island Press, Washington DC, 47-57. Lilley, S.A., Schiel, D.R., 2006. Community effects following the deletion of a habitat-forming alga from rocky marine shores. Oecologia 148, 672-681. Ling, S., Scheibling, R., Rassweiler, A., Johnson, C., Shears, N., Connell, S., Salomon, A., Norderhaug, K., Pérez-Matus, A., Hernández, J., 2015. Global regime shift dynamics of catastrophic sea urchin overgrazing. Philosophical Transactions of the Royal Society B: Biological Sciences 370, 20130269. Lõhmus, A., Lõhmus, P., 2010. Epiphyte communities on the trunks of retention trees stabilise in 5 years after timber harvesting, but remain threatened due to tree loss. Biological conservation 143, 891-898. Martin-Smith, K.M., 1993. Abundance of mobile epifauna: the role of habitat complexity and predation by fishes. Journal of Experimental Marine Biology and Ecology 174, 243-260. Marzinelli, E., Campbell, A., Vergés, A., Coleman, M., Kelaher, B.P., Steinberg, P., 2014. Restoring seaweeds: does the declining fucoid Phyllospora comosa support different biodiversity than other habitats? Journal of applied phycology 26, 1089-1096. Marzinelli, E.M., Leong, M.R., Campbell, A.H., Steinberg, P.D., Vergés, A., 2016. Does restoration of a habitat‐forming seaweed restore associated faunal diversity? Restoration Ecology 24, 81-90. McKenzie, P.F., Bellgrove, A., 2009. Dislodgment and attachment strength of the intertidal macroalga Hormosira banksii (Fucales, Phaeophyceae). Phycologia 48, 335-343. Meltcalfe, I., 2016. Phenological, physiological, and ecological factors affecting the epiphyte Notheia anomala and its obligate host Hormosira banksii. M.Sc. thesis, Biological Sciences, University of Canterbury, 131. Miller-Myers, R., Virnstein, R.W., 1999, Development and use of an epiphyte photo-index (EPI) for assessing epiphyte loadings on the seagrass Halodule wrightii. Seagrasses. CRC Press, pp. 133-142. Morton, J.E., Miller, M.C., 1973. The New Zealand Sea Shore. Collins, 500. Norton, T.A., Benson, M.R., 1983. Ecological interactions between the brown seaweed Sargassum muticum and its associated fauna. Marine Biology 75, 169-177. Parrish, D., 1977. Aspects of the Hormosira banksii-Notheia anomala relationship [parasite-host plant relation, Australia]. Australian Marine Science Bulletin. 18

Jo

ur

na

lP

re

-p

ro of

Pedersen, M.F., Filbee-Dexter, K., Norderhaug, K.M., Fredriksen, S., Frisk, N.L., Wernberg, T., 2019. Detrital carbon production and export in high latitude kelp forests. Oecologia, 1-13. Peery, M.Z., Kirby, R., Reid, B.N., Stoelting, R., Doucet-Beer, E., Robinson, S., Vasquez-Carrillo, C., Pauli, J.N., Palsboell, P.J., 2012. Reliability of genetic bottleneck tests for detecting recent population declines. Molecular Ecology 21, 3403-3418. Pinkerton, M., Lundquist, C., Duffy, C., Freeman, D., 2008. Trophic modelling of a New Zealand rocky reef ecosystem using simultaneous adjustment of diet, biomass and energetic parameters. Journal of Experimental Marine Biology and Ecology 367, 189-203. Ramus, A.P., Silliman, B.R., Thomsen, M.S., Long, Z.T., 2017. An invasive foundation species enhances multifunctionality in a coastal ecosystem. Proceedings of the National Academy of Sciences 114, 8580-8585. Reed, D.C., Rassweiler, A., Carr, M.H., Cavanaugh, K.C., Malone, D.P., Siegel, D.A., 2011. Wave disturbance overwhelms top‐down and bottom‐up control of primary production in California kelp forests. Ecology 92, 2108-2116. Rilov, G., Schiel, D.R., 2006. Seascape-dependent subtidal-intertidal trophic linkages. Ecology 87, 731-744. Russo, A.R., 1990. The role of seaweed complexity in structuring Hawaiian epiphytal amphipod communities. Hydrobiologia 194, 1-12. Schiel, D.R., 2006. Rivets or bolts? When single species count in the function of temperate rocky reef communities. Journal of Experimental Marine Biology and Ecology 338, 233-252. Schiel, D.R., 2011. Biogeographic patterns and long-term changes on New Zealand coastal reefs: Non-trophic cascades from diffuse and local impacts. Journal of Experimental Marine Biology and Ecology 400, 33-51. Schiel, D.R., Alestra, T., Gerrity, S., Orchard, S., Dunmore, R., Pirker, J., Lilley, S., Tait, L., Hickford, M., Thomsen, M., 2019. The Kaikōura earthquake in southern New Zealand: Loss of connectivity of marine communities and the necessity of a cross‐ecosystem perspective. Aquatic Conservation: Marine and Freshwater Ecosystems 29, 1520-1534. Schiel, D.R., Gerrity, S., Alestra, T., Pirker, J., Marsden, I., Dunmore, R.A., Tait, L.W., South, P.M., Taylor, D., Thomsen, M.S., 2018, Kaikoura earthquake: Summary of impacts and changes in nearshore marine communities. . Shaky Shores – Coastal impacts & responses to the 2016 Kaikōura earthquakes. New Zealand Coastal Society, pp. 25-28. Schiel, D.R., Hickford, M.J.H., 2001, Biological structure of nearshore rocky subtidal habitats in southern New Zealand. Science for Conservation, Department of Conservation. Schiel, D.R., Lilley, S.A., 2007. Gradients of disturbance to an algal canopy and the modification of an intertidal community. Marine Ecology Progress Series 339, 1-11. Schiel, D.R., Lilley, S.A., South, P.M., Coggins, J.H.J., 2016. Decadal changes in sea surface temperature, wave forces and intertidal structure in New Zealand. Marine Ecology Progress Series 548, 77-95. Schiel, D.R., Wood, S.A., Dunmore, R.A., Taylor, D.I., 2006. Sediment on rocky intertidal reefs: Effects on early post-settlement stages of habitat-forming seaweeds. Journal of Experimental Marine Biology and Ecology 331, 158-172. Schonbeck, M.V., Norton, T.A., 1979. Drought-hardening in the upper-shore seaweeds Fucus spiralis and Pelvetia peniculata. Botanica Marina 13, 199-217. Shaffer, M.L., 1981. Minimum population sizes for species conservation. BioScience 31, 131-134. Shears, N.T., Babcock, R.C., 2004, Community composition and structure of shallow subtidal reefs in northeastern New Zealand. Science for Conservation, Department of Conservation. Shi, X., Wang, Y., Liu-Zeng, J., Weldon, R., Wei, S., Wang, T., Sieh, K., 2017. How complex is the 2016 M w 7.8 Kaikoura earthquake, South Island, New Zealand? Science Bulletin 62, 309-311. Short, F.T., Wyllie-Echeverria, S.J.E.c., 1996. Natural and human-induced disturbance of seagrasses. Environmental Conservation 23, 17-27.

19

Jo

ur

na

lP

re

-p

ro of

Siciliano, A., 2018. Testing when and how habitat cascades control biodiversity of marine benthic ecosystems. PhD Thesis, University of Canterbury, 315. Sousa, W.P., 1979. Experimental investigations of disturbance and ecological succession in a rocky intertidal algal community. Ecological Monographs 49, 227-254. Stachowicz, J.J., 2001. Mutualism, facilitation, and the structure of ecological communities. BioScience 51, 235-246. Taylor, D., Delaux, S., Stevens, C., Nokes, R., Schiel, D., 2010. Settlement rates of macroalgal propagules: Cross-species comparisons in a turbulent environment. Limnology and Oceanography 55, 66. Taylor, D.I., Schiel, D.R., 2003. Wave-related mortality in zygotes of habitat-forming algae from different exposures in southern New Zealand: the importance of 'stickability'. Journal of Experimental Marine Biology and Ecology 290, 229-245. Taylor, D.I., Schiel, D.R., 2010. Algal populations controlled by fish herbivory across a wave exposure gradient on southern temperate shores. Ecology 91, 201-211. Taylor, R.B., 1997. Seasonal variation in assemblages of mobile epifauna inhabiting three subtidal brown seaweeds in northeastern New Zealand. Hydrobiologia 361, 25-35. Taylor, R.B., 1998. Short-term dynamics of a seaweed epifaunal assemblage. Journal of Experimental Marine Biology and Ecology 227, 67-82. Taylor, R.B., Cole, R.G., 1994. Mobile epifauna on subtidal brown seaweeds in northeastern New Zealand. Marine Ecology Progress series 115, 271-282. Tews, J., Brose, U., Grimm, V., Tielbörger, K., Wichmann, M., Schwager, M., Jeltsch, F., 2004. Animal species diversity driven by habitat heterogeneity/diversity: the importance of keystone structures. Journal of Biogeography 31, 79-92. Thomsen, M.S., Altieri, A.H., Angelini, C., Bishop, M.J., Gribben, P.E., Lear, G., He, Q., Schiel, D.R., Silliman, B.R., South, P.M., 2018. Secondary foundation species enhance biodiversity. Nature Ecology & Evolution 2, 634. Thomsen, M.S., Hildebrand, T., South, P.M., Foster, T., Siciliano, A., Oldach, E., Schiel, D.R., 2016a. A sixth-level habitat cascade increases biodiversity in an intertidal estuary. Ecology and Evolution, 113. Thomsen, M.S., McGlathery, K.J., Schwarzschild, A., Silliman, B.R., 2009. Distribution and ecological role of the non-native macroalga Gracilaria vermiculophylla in Virginia salt marshes. Biological Invasions 11, 2303-2316. Thomsen, M.S., Metcalfe, I., South, P., Schiel, D.R., 2016b. A host-specific habitat former controls biodiversity across ecological transitions in a rocky intertidal facilitation cascade. Marine and Freshwater Research 67, 144-152. Thomsen, M.S., Wernberg, T., 2005. What affects the forces required to break or dislodge macroalgae? A minireview. European Journal of Phycology 40, 1-10. Thomsen, M.S., Wernberg, T., Altieri, A.H., Tuya, F., Gulbransen, D., McGlathery, K.J., Holmer, M., Silliman, B.R., 2010. Habitat cascades: The conceptual context and global relevance of facilitation cascades via habitat formation and modification. Integrative and Comparative Biology 50, 158-175. Thornber, C., Jones, E., Thomsen, M., 2016. Epibiont-marine macrophyte assemblages. Marine Macrophytes As Foundation Species, 43-65. Tuya, F., Vanderklift, M., Wernberg, T., Thomsen, M.S., Hynes, G., Hanson, C., 2010. Proximity to edges impacts cross-habitat flows: implications for abundance patterns and species interactions. Marine Ecology Progress Series 405, 175–186. Tuya, F., Wernberg, T., Thomsen, M.S., 2009. Habitat structure affect abundances of labrid fishes across temperate reefs in south-western Australia. Environmental Biology of Fishes 86, 311-319. Underwood, A.J., 1997. Experiments in ecology - their logical design and interpretation using analysis of variance. Cambridge University Press, 504.

20

Jo

ur

na

lP

re

-p

ro of

Valentine, J.P., Johnson, C.R., 2005. Persistence of sea urchin (Heliocidaris erythrogramma) barrens on the east coast of Tasmania: inhibition of macroalgal recovery in the absence of high densities of sea urchins. Botanica Marina 48, 106-115. Vanderklift, M.A., Wernberg, T., 2008. Detached kelps from distant sources are a food subsidy for sea urchins. Oecologia 157, 327-335. Verling, E., Ruiz, G.M., Smith, L.D., Galil, B., Miller, A.W., Murphy, K.R., 2005. Supply-side invasion ecology: characterizing propagule pressure in coastal ecosystems. Proceedings of the Royal Society of London Series B: Biological Sciences 272, 1249-1257. Virnstein, R.W., 1999. Seagrass management in Indian River Lagoon, Florida: Dealing with issues of scale. Pacific Conservation Biology 5, 299-305. Wahl, M., 1989. Marine epibiosis I. Fouling and antifouling. Some basic aspects. Marine Ecology Progress Series 58, 175–189. Waters, J.M., Fraser, C.I., Hewitt, G.M., 2013. Founder takes all: density-dependent processes structure biodiversity. Trends in Ecology & Evolution 28, 78-85. Wernberg, T., Bennett, S., Babcock, R.C., Bettignies, T.d., Cure, K., Depczynski, M., Dufois, F., Fromont, J., Fulton, C.J., Hovey, R.K., Harvey, E.S., Holmes, T.H., Kendrick, G.A., Radford, B., SantanaGarcon, J., Saunders, B.J., Smale, D.A., Thomsen, M.S., Tuckett, C.A., Tuya, F., Vanderklift, M.A., Wilson, S., 2016. Climate driven regime shift of a temperate marine ecosystem. Science 353, 169172. Wernberg, T., Smale, D.A., Tuya, F., Thomsen, M.S., Langlois, T.J., de Bettignies, T., Bennett, S., Rousseaux, C.S., 2013. An extreme climatic event alters marine ecosystem structure in a global biodiversity hotspot. Nature Climate Change 3, 78-82. Wernberg, T., Vanderklift, M.A., How, J., Lavery, P.S., 2006. Export of detached macroalgae from reefs to adjacent seagrass beds. Oecologia 147, 692-701. Williams, J.C., Drummond, B.A., Buxton, R.T., 2010. Initial effects of the August 2008 volcanic eruption on breeding birds and marine mammals at Kasatochi Island, Alaska. Arctic, Antarctic, and Alpine Research 42, 306-314. Worm, B., Chapman, A.R.O., 1998. Relative effects of elevated grazing pressure and competition from a red algal turf on two post-settlement stages of Fucus evanescens C. Ag. Journal of Experimental Marine Biology and Ecology 220, 247-268.

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Figure 1. Study reefs at Cape Campbell (yellow circle: CC1 = ‘gate’, -41.734235, 174.275754; 338 photos before vs. 386 photos after; CC2 = ‘Lighthouse’, -41.725060, 174.276674; 250 vs. 328) and Kaikōura (yellow square: KK1 = ‘South Bay’, -42.427442, 173.691003; 181 vs. 483, KK2 = ‘Wairepo’, -42.421364, 173.713314; 162 vs. 358) on the South Island, New Zealand. These reefs were uplifted 0.5-0.8 m following an earthquake in Kaikōura on November 12, 2016. The red bar and number above the bar refer to ‘scale in metres’. Bottom photos show a reef prior to the earthquake (left) dominated by the canopyforming seaweed hosts Hormosira and Cystophora, and the same reef after the earthquake

Jo

ur

na

lP

re

-p

ro of

where seaweeds were decimated (right).

.

22

Figure 2. Percent cover of canopy-forming hosts (+ SE: A, B) and epiphytes (C, D) on four intertidal platforms on the South Island, New Zealand before (A, C) and after (B, D) reefs uplifted 0.5-0.8 m following a 7.8 Mw earthquake. Regions: CC = Cape Campbell (north), KK = Kaikōura (south), Reefs names: CC1 = ‘Gate’, CC2 = ‘Light house’. KK1 = ‘South Bay’, KK2 = ‘Wairepo’. The before-samples were collected in January 2015 and the aftersamples in February and March 2017. N = 338, 250, 181, and 162 (A, C: from left to right) and 386, 328, 483 and 358 (B, D: from left to right).

After uplift

Before uplift A. Hosts

B. Hosts

ro of

60

20

20

0

0 3

D. Epiphytes

3

C. Epiphytes

2

na

2

ur

1

0

re

40

-p

Hormosira banksii Cystophora torulosa Cystophora scalaris Cystophora retroflexa

40

lP

Percent cover

60

1

0 CC1 CC2 KK1 KK2

Jo

CC1 CC2 KK1 KK2

Notheia (on Hormosira) Reds (on Cystophora)

23

Figure 3. Population-level survival rates, where entire reefs are replicates (+SE, N = 4) following earthquake-related uplift, of canopy-forming fucoid hosts (Cystophora retroflexa, C. scalaris, C. torulosa, Hormosira banksii) and their epiphytes (Notheia anomala attached to Hormosira and various red algae, including Jania sphaeroramosa attached to Cystorphora spp.). Note that the y-axis is logarithmic.

ro of

10

1

-p

Survival (%)

100

re

0.1

0.01

Red

s

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lexa calaris mosira rulosa otheia f o r o N et C. s H or C. t C. r

24

Figure 4. Densities of invertebrates associated with canopy-forming seaweed hosts (+ SE; A, B) and their epiphytes (C, D) before (A, C) and after (B, D) the Kaikōura earthquake, standardized to number per gram dry weight of seaweed biomass. Horm = Hormosira banksii, C. tor = Cystophora torulosa, C. sca = C. scalaris, C. ret = C. retroflexa. N from left to right = 235, 13, 14, 9 (A), 30, 19, 31, 16 (B), 139, 20, 30, 6 (C) and 6, 3, 4, 3 (D). Densities were calculated from seaweed samples weighing, on average (from left to right) 5.4, 3.2, 2.5, 2.8 (A), 5.5, 3.2, 3.7, 2.8 (B), 5.8, 6.8, 3.2, 2.6 (C) and 2.4, 2.9, 2.5, 3.3 gram dry weight of the primary habitat-forming host and 0.00 (A, B, samples collected without epiphytes), 1.61, 1.81, 0,79, 0.61 (C) and 0.20, 0.03, 0.31 and 0.02 gram dry weight of secondary habitat-

ro of

forming epiphyte.

Before uplift 400

A. Hosts only

300

300 200

0

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na

Horm C. tor C. sca C. ret

400

'Others' Polychaetes Molluscs Crustaceans

100

lP

100

C. Hosts with Epiphytes

300

ur

Individuals per g DW

-1

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B. Hosts only

-p

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After uplift

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200

Horm C. tor C. sca C. ret

400 300 200

100

100

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Horm C. tor C. sca C. ret

D. Hosts with Epiphytes

Horm C. tor C. sca C. ret

25

Table 1. Three-factorial PERMANOVA testing for effects of earthquake associated uplift, canopy-forming fucoid seaweed host (Hormosira banksii, Cystophora torulosa, C. scalaris, C. retroflexa) and epiphytic seaweed (Epi: present-absent) on the abundance of mobile invertebrates (> 250 m) per gram of seaweed. Transformation did not achieve homogeneity of variances therefore significant results should be interpreted with caution. Alpha value for assessing significance was 0.01.

ur

na

Polychaetes

Other invertebrates

Jo

F 122.20 50.34 4.76 41.02 0.00 2.62 0.43

P 0.001 0.001 0.039 0.001 0.947 0.074 0.666

0.01 6.08 19.77 6.50 6.39 3.64 7.53

0.907 0.007 0.001 0.003 0.012 0.035 0.030

46.81 51.24 2.53 11.65 0.38 1.32 1.54

0.001 0.001 0.111 0.001 0.486 0.252 0.207

5.52 1.69 0.31 0.53 1.14 2.21 2.26

0.035 0.098 0.352 0.273 0.126 0.069 0.062

ro of

SS 471390 582580 18350 474700 19 30334 5026 2167900 11 17540 19009 18760 6147 10508 21736 540450 883 2900 48 659 7 75 87 10602 48 44 3 14 10 58 59 4878

-p

df 1 3 1 3 1 3 3 562 1 3 1 3 1 3 3 562 1 3 1 3 1 3 3 562 1 3 1 3 1 3 3 562

lP

Molluscs

Source Uplift Host Epi Uplift  Host Uplift  Epi Host  Epi Uplift  Host  Epi Residual Uplift Host Epi Uplift  Host Uplift  Epi Host  Epi Uplift  Host  Epi Residual Uplift Host Epi Uplift  Host Uplift  Epi Host  Epi Uplift  Host  Epi Residual Uplift Host Epi Uplift  Host Uplift  Epi Host  Epi Uplift  Host  Epi Residual

re

Response Crustaceans

26