Paper: “Earthquake-driven destruction of an intertidal habitat cascade”

Thomsen et al., 2020 Earthquake-driven destruction of an intertidal habitat cascadeMads S. Thomsen, Isis Metcalfe, Alfonso Siciliano, Paul M. South, Shawn Gerrity, Tommaso Alestra, David R. Schiel



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 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 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 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.

Thesis: “Testing when and how habitat cascades control biodiversity of marine benthic ecosystems”

Siciliano thesis

Alfonso Siciliano, Mads S. Thomsen, David R. Schiel



The important role of indirect facilitation, like trophic cascade and keystone predation, in structuring communities have been documented over many decades and across ecosystems. By contrast, indirect facilitation mediated by habitat cascades (where ‘inhabitants’ organisms are facilitated through sequential habitat formation or modification) is less studied, and these processes are not covered in ecological text books or conservation practices. This could be because habitat cascades are ecologically unimportant, or, alternatively, highlights a major research gap.

In this thesis, I investigated the core hypothesis that habitat cascades can be key drivers of biodiversity in marine benthic ecosystems. To test this hypothesis, I combined descriptive and experimental field and laboratory studies aimed at improving our understanding of the mechanisms underpinning habitat cascades via three broad research objectives: (i) quantifing the variability in habitat cascades under different environmental conditions, (ii) testing mechanisms that increase or decrease habitat cascades, (i) testing how habitat cascades can be affected by human stressors.

In Chapter 2, I described two new habitat cascades from relatively ‘simple’ sedimentary estuarine shell beds, where small infaunal bivalves (Austrovenus stutchburyi, primary habitat former) provide substrate for large and form-functionally different seaweeds (Ulva sp. and Gracilaria chilensis, secondary habitat formers). To date, most research on habitat cascades has focused on interactions between a single primary and secondary habitat former studied on small spatio-temporal scales, thereby questioning if habitat cascades have broad ecological relevance. I tested if habitat cascades, when standardized by seaweed biomass, are stronger at high than low abundances of the secondary habitat former and when the secondary habitat former has high (Gracilaria) compared to low (Ulva) morphological complexity. I also tested if habitat cascades are stronger at higher latitudes, where intertidal desiccation stress is stronger, and when secondary habitat formers are alive compared to mimics. In contrast to my hypotheses, I found weaker habitat cascades at high abundances and for the coarsely branched habitat formers, and I found no patterns across latitudes; however, as expected I did find stronger habitat cascades for living than mimic of secondary habitat formers.

Chapter 3 described, from the same estuarine sedimentary system, a rare example of a ‘higher-level habitat cascade’. Virtually all habitat cascade studies have tested if and how two co-occurring habitat-forming species affect biodiversity compared to systems dominated by a single habitat-forming species. My aim here was to document a new ‘long habitat formation cascade’ where the primary bivalve Austrovenus provides attachment space for the secondary seaweed Gracilaria, that again provides substratum for the tertiary epiphytic seaweed Ulva. I tested if this long bivalve-seaweed-seaweed cascade affected mobile invertebrates and if it is a general process operating across Gracilaria biomasses, seasons, elevation levels, sites and estuaries. My study confirmed that Ulva increased invertebrate abundances and altered community structures, whereas increases in taxonomic richness only was observed under a smaller subset of environmental conditions. These positive effects were, however, not supported for non-living Ulva mimics, suggesting that common invertebrates graze on Ulva.

In Chapter 4 I described a new habitat cascade from a seagrass-dominated system where unattached seaweeds (Ulva, secondary habitat former) can become entrapped and entangled around seagrass leaves (Zostera muelleri, primary habitat former). I tested the hypotheses that (i) the presence of seaweeds entangled in estuarine seagrass beds modify biodiversity via cascading habitat formation, (ii) similar processes occur across a wide range of spatial and temporal conditions, and (iii) the biomass and the structural attributes of seaweeds (comparing living vs artificial mimics) modify the strength of habitat cascades. I found that entangled seaweeds, across latitudes, elevation levels and seasons, consistently increased the abundance and richness of invertebrates and I also found stronger facilitation of invertebrates in high than low seaweed biomass and by live than mimic seaweeds. Furthermore, an experiment, using different seaweed mimics showed consistent facilitation of invertebrates with increasing mimic biomass between estuaries and across latitudes, thereby supporting all three hypotheses in a single experiment. I concluded that entangled seaweeds, by adding biomass and different physical structures, can support strong habitat cascades in sedimentary estuarine seagrass beds.

In Chapter 5 I tested, again in a seagrass-dominated system, if and how anthropogenic stressors, like fertilization and enhanced sedimentation, affect seagrass performances and seagrass-seaweed habitat cascades. I found that fertilization had little impact whereas even low sedimentation levels had strong negative effects on both seagrass and fauna. Furthermore, I found strong negative effects of sediments, across seasons and elevation levels, but also that negative effects of sediments on invertebrates were elevated in the presence of the secondary habitat former. These results thereby provide rare evidence of how a habitat cascade can break down under high anthropogenic stress.

In Chapter 6, I studied habitat cascades from more diverse rocky intertidal shores. Primary habitat formers with different morphologies affect secondary habitat-forming epiphytes and epifauna differently. However, no studies have tested the opposite hypothesis; do morphologically ‘similar’ congeneric primary habitat formers support similar epiphytes with similar direct and indirect cascading effects on invertebrate communities? This hypothesis was tested by sampling co-existing congeneric habitat-forming fucoid seaweeds, Cystophora torulosa, C. scalaris, and C. retroflexa, with and without epiphytes across reefs and latitudes. The survey was then followed by field experiments, where defaunated Cystophora species and the morphologically different fucoid Hormosira banksii, with and without living and mimics of epiphytes, were out-transplanted to quantify the impact on colonizing gastropods. I found that the three Cystophora species supported different gastropod communities and had different cascading effects, and that these results can be, in part, explained by their physical structures. I also found that epiphytic biomass had strong positive effect on gastropods abundances, and that artificial mimics and live epiphytes were colonized by similar gastropod communities, suggesting that structural effects are more important than whether the habitat is ‘edible’.

In Chapter 7, I tested, again from rocky intertidal systems, if habitat cascades affect secondary (animal) production. Secondary production of small mobile invertebrates inhabiting Cystophora seaweed, with and without epiphytes, was estimated from published productivity models. More specifically, I tested if (i) the three Cystophora species support similar secondary production, (ii) finely branched epiphytes increase secondary production, (iii) production is greatest in warmer locations and seasons, and (iv) secondary production is higher on living epiphytes than non-living epiphyte mimics. The first two hypotheses were rejected as the three Cystophora species supported different secondary production and because epiphytes, when its biomass was taken into consideration, did not increase secondary production. Nevertheless, the two latter hypotheses were both supported, as production was highest in the northern location and in summer months and on living than mimic epiphytes. Thus, similar looking congeneric primary habitat formers supported different secondary production and epiphytes did not increase secondary production per seaweed-biomass, but will increase areal-based production when epiphytes enhance total standing plant biomass.

I conclude that poorly studied habitat cascades were ubiquitous in marine benthic systems on the South Island of New Zealand, modifying animal biodiversity across habitats, seasons, years, latitudes, sites and elevations levels. I also conclude that data on the abundances, morphologies and types (live or not) of co-existing habitat formers were strong mechanistic descriptors of habitat cascades. I finally suggest that habitat cascades, like other important indirect facilitation processes, should be covered in ecological text books and conservation practices.

Paper: “Effects of local anthropogenic stressors on a habitat cascade in an estuarine seagrass system”

Siciliano et al., 2019 Effects of local anthropogenic stressors on a habitat cascade in an estuarine seagrass system_1

Alfonso Siciliano, David R. Schiel and Mads S. Thomsen



Recent research has shown that co-occurring primary and secondary habitat-forming species typically support higher biodiversity than do monocultures of the primary habitat-former alone. However, these ‘habitat cascades’ may not be universal and it is important to know whether, when and where positive effects on biodiversity from secondary habitat-forming species change to negative effects. Here, we tested how anthropogenic stressors (fertilisation and sedimentation) and unattached secondary habitat-forming Ulva seaweeds affected the primary habitat-forming seagrass, Zostera muelleri, and its associated invertebrates in the Avon–Heathcote Estuary, New Zealand. We experimentally stressed Zostera by adding different fertilisation and sediment levels. Fertilisation had little impact, whereas even low sedimentation levels had strong negative effects on Zostera and its associated fauna. In a second experiment, sediments and Ulva were added to seagrass beds and unvegetated mudflats to test whether sediment stress modifies habitat cascades. We found again strong negative effects of sediments on Zostera, irrespective of spatio-temporal conditions, and that negative effects of sediments on invertebrates were enhanced in the presence of the secondary habitat former. These results highlighted that anthropogenic stressors can destabilise habitat cascades; processes that may be of particular importance in estuaries that are characterised by low biodiversity and stressful environmental conditions.

Conference: “Host variety enhances diversity: the role of multiple secondary habitat-forming seaweeds in facilitating estuarine invertebrate communities”

New Zealand Marine Science Society conference (NZMSS) 2017, University of Canterbury, New Zealand

10-nzmss-2017 2

Alfonso Siciliano, Mads S. Thomsen, David R. Schiel



Shell-forming molluscs are primary habitat-forming species that affect the structure of invertebrate assemblages in sedimentary estuaries. Importantly, their shells provide hard substratum that seaweeds attach to, and these seaweeds can subsequently provide secondary habitat to epibiontic invertebrates, giving rise to habitat cascades. Here we hypothesized that (1) invertebrate communities depend on the identity and density of morphologically different seaweeds (Gracilaria chilensis vs. Ulva sp.), (2) these invertebrates have different host-specificities related to the ecological differences between seaweeds, (3) results are consistent across latitudes and (4) invertebrate community structure depends on whatever primary and secondary habitat-formers are alive or dead (mimics). The first two hypotheses were tested in surveys and experiments run seasonally. There were consistent significant effects of both seaweed species-identity and density, but the results from the experiment was less conclusive. A regional survey in 13 estuaries tested the third hypothesis, confirming the results from the local survey. Finally, a field experiment confirmed hypothesis four demonstrating that live habitat-formers have higher diversity than mimics, suggesting that secondary habitat-formers may provide trophic subsidies for invertebrates. In concert, these results show that habitat cascades are common in increasing biodiversity in estuaries of the South Island of New Zealand.

Conference: “Habitat cascade destroyed in the Kaikoura earthquake”

New Zealand Marine Science Society conference (NZMSS) 2017, University of Canterbury, New Zealand


Mads S. Thomsen, Isis Metcalfe, Alfonso Siciliano, Tommaso Alestra, Stacie Lilley, Shawn Gerrity, David R. Schiel



It is well-described how anthropogenic activities and natural disaster can destroy primary habitat-forming species, like seagrasses, corals and kelps. However, less research and conservation effort has focused on how these types of disturbances affect associated secondary habitat-formers, like epiphytes, and animals depending on biogenic habitat. In this talk we will first introduce the concept of habitat cascades with examples from New Zealand rocky shores and compare them to habitat cascades from other ecosystems. We will then show that intertidal primary (fucoid hosts) and secondary (seaweed epiphytes) habitat-formers and their inhabitants (small mobile invertebrates) have been decimated on reef along a 100km swathe of coastline that were uplifted by 1-6m by the recent 7.8mW Kaikoura earthquake. Finally, we will discuss potential cascading ecological effects, future scenarios for natural recovery and whether restoration is a viable option to speed up the recovery of habitat cascades on these degraded reefs.

Paper: “Recreational diving and its effects on the macroalgal communities of the unintentional artificial reef Zenobia shipwreck (Cyprus)”


Alfonso Siciliano, Jimenez Carlos, Antonis Petrou



The ecological role of shipwrecks as artificial reefs is well established and often is prime and exclusive destinations for diving tourism. But they are also extremely delicate and sensitive environments. For this reason, the impact of recreational diving on shipwrecks should be taken in consideration since diver’s experience can strongly affect their associated benthic communities. The aim of this study was to verify the impact of anthropogenic activities (scuba divers) on the macroalgal coverage, here considered as indicator of physical disturbance, on the modern shipwreck Zenobia, in Cyprus (east Mediterranean Sea). Divers behaviour was investigated in the wreck and the macroalgal coverage was determined (photo-quadrat method) in three areas differently exposed to physical contact of divers. Our results suggest that diving is having a significant negative effect on the macroalgae coverage of the shipwreck, especially in areas subject to high levels of use (e.g., meeting stations) when compared to control sites in the same wreck. Divers’ behaviour and popular dive routes at the wreck are factors associated to the observed decrease in macroalgae benthic cover. It is important that relevant stakeholders utilizing the Zenobia wreck agree on basic management planning in order to protect and enhance the wreck’s biodiversity. In addition, this study provides for the first time evidence of ecological deterioration of one of the most emblematic shipwreck of the Mediterranean Sea.

Conference: “Effects of seaweeds, nutrients and sedimentation on seagrass and seagrass-associated fauna”

Annual Biology Conference (ABC) 2016, University of Canterbury, New Zealand


Alfonso Siciliano, Mads S. Thomsen, David R. Schiel



Seagrasses are marine plants that take up nutrients, stabilize sediments, increase habitat complexity and thereby also increase biodiversity of sedimentary coastal ecosystems. Seagrasses also facilitate seaweeds that can become entangled around seagrass leaves and stems. However, relatively little is known about interactions between entangled seaweeds and seagrass, their effects on seagrass-associated invertebrates and if their interactions are modified by abiotic conditions, like nutrient and sedimentation levels. We aimed to test the hypotheses that (i) seaweeds have negative effects on seagrass (competing for limited resources) but positive effect on invertebrate biodiversity (by increasing habitat-complexity), across seasons in the Avon-Heathcote estuary, (ii) that similar processes occur in other estuaries, and (iii) that the magnitude of effects increases with increasing levels of inorganic nutrients and sediments. To test the first two hypotheses, we collected cores from the Avon-Heathcote estuary and from six other estuaries. To test the third hypothesis, we manipulated nutrient and sedimentation levels in two field-experiments. Preliminary data analysis supports our hypotheses: seaweeds had negative impact on seagrass but positive effects on the abundance of many invertebrates. We also found that enhanced sediments, but not nutrients, had strong negative impact on seagrass with cascading negative impacts on the invertebrate community.

Paper: “A sixth-level habitat cascade increases biodiversity in an intertidal estuary”


Mads S. Thomsen, Thomas Hildebrand, Paul M. South, Travis Foster, Alfonso Siciliano, Eliza Oldach, David R. Schiel



Many studies have documented habitat cascades where two co-occurring habitat-forming species control biodiversity. However, more than two habitat-formers could theoretically co-occur. We here documented a sixth-level habitat cascade from the Avon-Heathcote Estuary, New Zealand, by correlating counts of attached inhabitants to the size and accumulated biomass of their biogenic hosts. These data revealed predictable sequences of habitat-formation (= attachment space). First, the bivalve Austrovenus provided habitat for green seaweeds (Ulva) that provided habitat for trochid snails in a typical estuarine habitat cascade. However, the trochids also provided habitat for the non-native bryozoan Conopeum that provided habitat for the red seaweed Gigartina that provided habitat for more trochids, thereby resetting the sequence of the habitat cascade, theoretically in perpetuity. Austrovenus is here the basal habitat-former that controls this “long” cascade. The strength of facilitation increased with seaweed frond size, accumulated seaweed biomass, accumulated shell biomass but less with shell size. We also found that Ulva attached to all habitat-formers, trochids attached to Ulva and Gigartina, and Conopeum and Gigartina predominately attached to trochids. These “affinities” for different habitat-forming species probably reflect species-specific traits of juveniles and adults. Finally, manipulative experiments confirmed that the amount of seaweed and trochids was important and consistent regulators of the habitat cascade in different estuarine environments. We also interpreted this cascade as a habitat-formation network that describes the likelihood of an inhabitant being found attached to a specific habitat-former. We conclude that the strength of the cascade increased with the amount of higher-order habitat-formers, with differences in form and function between higher and lower-order habitat-formers, and with the affinity of inhabitants for higher-order habitat-formers. We suggest that long habitat cascades are common where species traits allow for physical attachment to other species, such as in marine benthic systems and old forest.

Conference: “Epiphytism as key driver of biodiversity in canopy-forming seaweeds-dominated systems”

11th International Temperate Reefs Symposium (ITRS) 2016, University of Pisa, Italy


Alfonso Siciliano, Mads S. Thomsen, David R. Schiel



It is well established that host species that are morphologically and genetically different can support different epibiotic species, and that these differences can support different invertebrate communities. However, no studies have tested the opposite hypothesis of whether morphologically similar congeneric hosts support similar epibiota and have similar cascading effects on invertebrate communities. This hypothesis was tested with mensurative and manipulative experiments using three conspecific, morphologically similar marine seaweed hosts: the canopy-forming fucoids Cystophora torulosa, C. scalaris, and C. retroflexa. In the mensurative experiment, hosts, epiphytes and associated invertebrate communities were sampled and enumerated from 4 tide-pools (>1 m apart), at 2 reefs (>1 km apart) and 4 sites (>100 km apart). In two follow-up manipulative experiments, defaunated hosts, epiphytes and epiphytes’ mimics were combined and transplanted to shared tide pools and the epifaunal recolonization was quantified. Both experiments suggest that epiphytism increases abundances and richness of invertebrates, across host species, epiphyte species, sites, regions, and experimental methods, demonstrating its key role in sustaining the epifaunal community. However, the experiments reject the initial hypothesis since congeneric and morphologically similar hosts appear to support a different epifauna and having different cascading effects.