Overview: what is a habitat cascade?

‘Habitat cascade’ or ‘cascading habitat-formation’ and/or ‘cascading habitat-modification’

A habitat cascade is a common type of a facilitation cascade 1,2 where “indirect positive effects on focal organisms are mediated by successive formation or modification of biogenic habitat” 3. A habitat cascade is composed of at least three organisms: a primary (hereafter 1st) habitat-former or modifier; a secondary (hereafter 2nd) habitat-former or modifier; and a focal organism that utilizes the secondary habitat-former or modifier. For example, 1st habitat-forming trees can provide habitat for 2nd habitat-forming epiphytes, lianas or vines that again can provide habitat to focal organisms like insects and birds 4. The 1st and 2nd habitat-formers has also been called ultimate and proximate habitat-formers 5, basal and intermediate habitat-formers 3, 1st and 2nd ecosystem engineers 6, 1st and 2nd foundation species 7, basibionts and epibionts 8, basizoids (if animal) or basiphytes (if plant) and epizooids (if animal) or epiphytes (if plant) 8, hosts and structural parasites 9 or 1st and 2nd fouler 10. Focal organisms have been referred to as clients, end-users, habitat-users, inhabitants and hyperepibionts 3,11,12.

Secondary habitat-formers can be attached to 13, entangled around 14 or embedded within 15 the 1st habitat-former. Habitat cascades are strongest when the 2nd habitat-former is more effective than the 1st habitat-former at allowing focal organisms to avoid stress and enemies, and find resources and other facilitators 11.

Habitat cascades can increase biodiversity in ecosystems dominated by structural organisms that are large, long-lived, and sessile or slow-moving 11. For example, increases in biodiversity associated with habitat cascades have been documented in tropical 16 and temperate forests 4, salt marshes 1, coral reefs 17, seagrass beds 14, mangrove stands 18, polychaete gardens 3, seaweed-covered rocky coasts 13, and molluscan communities 15.

Most research in our lab focuses on habitat-formers as controllers of cascading habitat-formation and modification. Common alternative ecological terms often used as synonyms to habitat-formers include “ecosystem engineers” 19, “foundation species” 20, and “structural species” 21. We generally frame our research around “habitat-formation” for reasons of (i) history (habitat is a very old term in biology) 22, (ii) simplicity (habitat is defined in primary to tertiary educational biology text books), (iii) precision (many studies only quantify where habitat-formers and inhabitants are found, not what they do), (iv) to reduce ambiguity (e.g., the phrase ‘‘biogenic habitat-formation by ecosystem engineers’’ is almost tautological), (v) to avoid overlap in definitions (definitions of ecosystem engineers or foundation species often differ between researchers and change over a short time) and finally (iv) because our research typically target effects on the abundances, distribution and community structure of inhabitants 20,23-25. Most of our empirical research focuses on the processes that control the strength of habitat cascades in the photic zone of rocky and sedimentary ecosystems.

Fig. 1. Habitat cascades from rocky shore (left) and sedimentary estuary (right). Red circle = 1st habitat-former (turf alga vs. cockle), Green = 2nd habitat-former (kelp holdfast vs. Gracilaria seaweed); Yellow = inhabitants (snail vs. crab). The snail attached to the holdfast (left) is also covered by encrusting red alga which again is inhabitated by a small black limpet (i.e., a long habitat cascade). Habitat cascades from rocky shores are, compared to habitat cascades from estuaries (a) of higher diversity (there are more habitat-forming species), (b) ecologically less important (habitat-forming species can attach directly to rock instead of biogenic substrates) and (c) typically size structures (because waves dislodge large habitat-formers).

Chronology over published habitat cascade research from ‘Thomsenlab’

1. Habitat cascades and early field observations; Diopatra and Gracilaria as ‘ultimate’ and ‘proximate’ habitat modifiers 5

Our initial interest in habitat cascades was inspired from field work on temperate intertidal mudflats in the West Atlantic 26. Surveys on these mudflats showed that the dominant primary producer, the invasive red seaweed Gracilaria vermiculophylla27 was facilitated by a ‘gardening’ polychaete (Diopatra cuprea) 5. This polychaete collects Gracilaria and uses a glue to incorporate seaweed fronds to the part of its tube that protrudes above the sediment surface. The polychaete does this to eat the seaweed, eat the small invertebrates that are associated with Gracilaria, hide from predators and reduce environmental stress during low tide. Several studies have shown that Gracilaria itself provides habitat to many sessile 5 and mobile 28 species. This suggests that a chain of positive interactions could control biodiversity in these systems, as Diopatra facilitates Gracilaria through habitat provisioning, and Gracilaria subsequently facilitates sessile and mobile species, again through habitat provisioning. More specifically, we showed that in Virginia, habitat-forming seaweeds (e.g. Ceramium, Hypnea and Champia) and sessile animals (e.g. the bryozoan Bulgula) were ‘secondarily attached’ to Gracilaria which was again was incorporated into the Diopatra tubes 5. Therefore, we defined Gracilaria and Diopatra as ‘proximate’ and ‘ultimate’ habitat modifiers that controlled biodiversity 5. We also speculated that longer habitat cascades could occur, as Diopatra facilitates Gracilaria that then facilitates Ceramium that potentially again facilitates small invertebrates.

Fig. 1.1. A. Estuarine mudflat without biogenic habitat-formers. B. Mudflat converted to a meadow of scattered patches of seaweeds of the invasive red alga, Gracilaria vermiculophylla (a patch encircled in yellow). C. Close-up of seaweed patch with a ‘humps’ around each patch. D. A patch where the tube of the gardening polychaete Diopatra (1st habitat-former that incorporate the 2nd habitat-former). D-insert. Close-up of Diopatra polychaete that is partly out of its tube (encircled).

2. Habitat cascades can spill-over to adjacent ecosystems 29

In this paper we hypothesized that habitat cascades can be important beyond the system where the 1st habitat-former provides habitat to the 2nd habitat-former. To test the hypothesis we followed tagged Gracilaria (2nd habitat-former) attached to Diopatra tubes (1st habitat-former) on mudflats in Virginia, USA. We showed that, during storms and peaks in tidal currents, Gracilaria fronds were transported to adjacent salt marshes together with their associated sessile and mobile inhabitants 29. Within the marshes, Gracilaria became entangled around Spartina stems (the new 1st habitat-former) and was thereby stabilized from further movement by tidal currents and waves. After deposition, the marine stenohaline organisms (e.g., Hypnea seaweeds and Caprella and Pagarus crustaceans) that inhabited Gracilaria on the mudflats disappeared rapidly, but more tolerant euryhaline inhabitants (Ulva, several polychaetes) survived. Gracilaria also became colonized by a new suit of saltmarsh inhabitants such as Bostrychia seaweeds, Hydrobia snails and saltmarsh crabs. We also showed that in both Diopatra mudflats and salt marshes, the 2nd habitat-former provided nursery function for juvenile fish (killifish and silversides) and commercially important juvenile blue crabs29.

Fig. 2.1. Seaweeds mats (the invasive Gracilaria vermiculophylla) grow in polychaete gardens on intertidal mudflats (left) but dislodges during storms, and are transported to adjacent saltmarshes (right) where new invertebrate communities colonize this novel habitat.

3. Defining habitat cascades, how they are measured, and their commonality in nature 3

The objective of our next paper 3 was fourfold:

(1) to define the habitat cascade and conceptualize habitat cascade in a context of indirect positive effects associated with sequential species-interactions between at least 3 interacting organisms;

(2) to review published examples of habitat cascades across ecosystems, and present new examples from soft-bottom estuaries, to document that habitat cascades are general ecological phenomena;

(3) to propose a standardized terminology and metrics that allowed us to compare habitat cascades across studies, ecosystems and environmental conditions;

(4) to discuss how human activities modify habitat cascades and outline research topics that will increase our understanding of ecosystems by incorporating habitat cascade ecology.

Building on our early research 5, we defined a common type of species association, which did not have a name and which had not been studied much. Facilitation cascades have previously described processes “in which the positive effects of a secondary facilitator are contingent on habitat amelioration by a primary foundation species” 1. Facilitation was here used in a context of positive effect of one species on another species, regardless of possible negative feedbacks, because the study did not test how inhabitants affected the habitat-formers 1,30. However, other researchers define facilitation as a process that benefits at least one of the participants and causes harm to neither, perhaps to avoid conflating facilitation with consumption processes 31-33. This definition therefore requires that the effects of inhabitants on habitat-formers are quantified and that these effects are neutral or positive (corresponding to commensalism and mutualism, respectively). Furthermore, this definition of a facilitation cascade requires proof that the 1st species ‘ameliorates the habitat’ for the 2nd species. Habitat-amelioration is typically analysed in the context of reduction in stressors 33-35, but stress-reduction requires experimental approaches to verify and does not encompass common neutral processes, such as ‘epibiosis’ (where the 2nd species simply attaches to the surface on the 1st species) or ‘entanglement. So, to unify and compare the many studies that only quantify distribution and abundance of organisms in samples but that do not test for reciprocal ecological interactions (or habitat-ameliorating processes), we defined the habitat cascade as “indirect positive effects on focal organisms mediated by successive facilitation in the form of biogenic formation or modification of habitat”. In habitat cascade studies it does not matter whether positive or negative feedbacks occur on the 1st or 2nd habitat-formers. It only requires that 1st and 2nd species provide habitat – that is, a place for other organisms to live in, on or around. Relevant studies therefore include both those studies that simply quantify ‘where organisms live’ (habitat-formation) as well as the more complex studies that quantify ‘why organisms live where they do (because of habitat modifications, including stress-amelioration). Habitat cascades can therefore be quantified simply from observations and collections of samples of the 1st and 2nd habitat-formers. Unmeasured possible reciprocal trophic interactions do not matter in this definition: for example, mistletoes and herbivorous inhabitants are ’allowed’ to extract trophic subsidies from the biogenic habitat they live on, without invalidating the presence of the habitat cascade. Following this definition, we highlighted that four fundamental ecological processes represent most direct species interactions: habitat-formation (positive effect); mutualism (positive effect); competition (negative effect); and consumption including parasitism, grazing, and predation (negative effects). These four processes result in eight forms of indirect positive effects when combined for three-species interaction chains (Fig. 3.2 for details), where cascading habitat-formation probably is the most simple to measure.

Fig. 3.1. A hypothetical biogenic habitat cascade. Biogenic = produced by living organisms. Habitat = place where an organism normally occurs. Cascade = succession/sequence of stages, processes, or units. A biogenic habitat cascade is composed of a matrix, and at a minimum a basal (1st) habitat, intermediate (2nd) habitat and focal organisms (inhabitants) (with more co-occurring habitat-formers in long habitat cascades). Matrix = ground substance (here soil and air) in which things (here organism) are embedded. Basal habitat-former = primary habitat; here tree. Intermediate habitat-former = secondary habitat; here climbing vine. Focal organisms = inhabitants = dependent variables; here birds and insects. Focal organisms will, at any given time, be sampled or observed within the matrix, or the 1st or 2nd habitats. Inhabitants only found in a single habitat = obligate; here earthworm and parrot in soil and air matrix, longhorn beetle and magpie in tree, and finch and bee in vine. Inhabitants found in multiple habitats = facultative; here ladybirds and ants. Most organisms in real habitat cascades are facultative with different affinities for different habitats. Units of habitat cascades are repeated in space (trees to forest, forest to shrubs or grassland) with widely different proportions of habitat-formers and inhabitants.

Second, we conducted a literature review identifying published case studies on habitat cascades from terrestrial and marine ecosystems. This review distinguished between cascades in which the 2nd habitat-former is physically attached or incorporated onto the 1st HF (= ‘epibiosis’, e.g., as epiphytes) and cascades in which the 2nd habitat-former is embedded within the 1st habitat-former (as in Altieri). We also presented our own empirical experimental and survey data from soft-bottom estuaries to document very different but ubiquitous habitat cascades in estuarine systems across four continents. These estuarine examples differed from past habitat cascade case studies because relatively small invertebrates (a gardening polychaete, a burrowing bivalve, a surface dwelling bivalve, and a bioturbating snail) rather than primary producers were 1st habitat-formers. The primary producers, in the case of these examples, were the larger 2nd habitat formers. Our results showed strong positive effects of 2nd habitat-formers on biodiversity (taxonomic richness and population abundances) for both mobile and sessile inhabitants (some of which may in turn be involved in longer habitat cascades). This pattern held across sites, continents, and different types of 1st habitat-forming invertebrates.

Third, we standardized and summarized generalities of habitat cascades using a ‘Magnification Ratio’ (MR). MR compares an attribute of the model system in the co-occurrence of the 1st + 2nd HF (“treatment”) to the attribute when 1st HF exists alone (“control”). Ln MR corresponds to the ‘Log Response ratio’, a formal effect size commonly used in meta-analyses. After computing MR for our experiment, we extracted data from the reviewed literature and calculated MR values from past case-studies across ecosystems and habitats. We documented that MR values typically exceeded 1, meaning there is typically a positive net effect on biodiversity in the presence of a 2nd habitat-former. We also highlighted the importance of distinguishing between studies showing how a single or few species or form-functional groups are affected in habitat cascade versus studies showing community-wide impacts. This is a distinction also emphasized for the study of trophic cascades. We then discussed how sampling techniques varied between studies, and the potential of sampling technique for modifying the MR values. For example, sampling an entire tree versus a branch with or without epiphytes, or sampling co-existing habitat-formers with or without inclusion of the abiotic matrix.

Finally, we discussed human impacts and outlined future research that will allow a better understanding of ecosystems by incorporating concepts about habitat cascades. We first provided examples on how invasions, pollution, climate changes and habitat destruction can affect both 1st and 2nd habitat-formers and that in order to better understand human impacts, co-existing habitat-formers need to be managed in concert (not just focusing on the more visible 1st habitat-formers). We also outlined the need to test the hypotheses that habitat cascade effects are stronger when: the 2nd habitat former is larger and more abundant (amounts matters); the 2nd HF is -functionally different from the 1st habitat-former (differences in traits matter); and inhabitants have high host-specificity for 2nd habitat-formers (affinity matters). These research questions were later summarized as the ‘ADA habitat cascade hypothesis’ 13. We also hypothesized that (as also suggested for trophic cascades) on larger scales, spatial heterogeneity, increasing complexity of the food-web, and presence of interspersed alternative habitats will reduce magnification ratios due to diffusion and substitution of inhabitants to alternative pathways and habitats.

Fig. 3.2. Habitat cascades compared to other indirect positive effects arising from three organisms interacting in succession. We changed the terminology of a few well-known interaction chains to highlight that two positive (habitat-formation and mutualism) and two negative (competition and consumption) processes cause 8 forms of indirect positive effects. Habitat-formation and mutualism are not mutually exclusive, but emphasize different processes and different requirements regarding feedback mechanisms (compare examples A and B). Indirect positive effects are caused by direct positive effects between organisms in example A–D (= a friend of my friend is my friend) and direct negative effects in example E–H (= an enemy of my enemy is my friend). The first four examples represent facilitation cascades in its broadest meaning (facilitation = positive effect of species 1 on species 2 regardless of species 2’s effect on species 1). Example A shows the habitat cascade that is characterized by ‘‘successive biogenic habitat-formation’’ or modification between organisms. Example B is a mutualism cascade in which focus is on ‘‘successive mutualism’’ (or commensalism, i.e., corresponding to facilitation in its strict ecological definition). Examples C and D combine processes of mutualism and habitat-formation. Example C can occur when non-habitat-forming pollinators, seed-dispersers, cleaners, protectors, or C/N-fixers such as symbiotic dinoflagellates or mychorrhiza, facilitate habitat-formers, like trees or corals. This chain of interactions is called keystone mutualism, because a keystone species causes disproportionately large effects compared to its abundance or biomass. In example D, a habitat-former provides living space for an organism that is involved in mutualism with a focal organism. Thus, a tree can provide habitat for a bee nest, and the bees can pollinate adjacent flowering plants. This process is referred to as keystone habitat-formation, because the importance of habitat-formation extends beyond the direct effects on the intermediate organisms. The last four examples represent enemy cascades (successive enemy interactions). Example E is a competition cascade, i.e., with ‘‘successive competition’’ between organisms. Competition cascades occur in assemblages in which pairs of competitors compete for different resources. Example F is a consumption cascade, i.e., with ‘‘successive consumption’’ between organisms (= trophic cascades, emphasizing that interacting organisms occupy successive trophic layers). Example G shows keystone consumption, a chain that starts with consumption and is followed by competition. In keystone consumption a predator or grazer consumes a dominant competitor, thereby indirectly facilitating an inferior competitor (typically referred to as keystone predation). Finally, example H shows keystone competition, a competitor reduces the performance of a consumer with indirect positive effects on the prey. Note that example B, E, and F result in reciprocal indirect positive feedbacks from the 3rd organisms back to the 1st organism. These three examples therefore also represent examples of ‘indirect mutualisms’, as both the 1st and 3rd organisms benefit from indirect effects.

4. Habitat cascades: controlled by the amounts of the secondary habitat-formers – with different effects on different inhabitant taxa and life-stages in different environments 14

For this paper there were three aims: (1) to follow up on the hypothesized ‘ADA’ model 3 testing if the amount of the 2nd habitat-former increases the strength the habitat cascade; (2) to test if results were consistent between juvenile and adult inhabitants, for different inhabitant taxa and in different environments (two depth levels); and (3) to show data from a habitat cascade characterized by ‘entanglement’, rather than incorporation, between 1st and 2nd habitat formers. A previous study had shown that Gracilaria seaweeds can be commonly entangled around the seagrass stems in seagrass beds 36, analogues to how Gracilaria entangles around Spartina stems in salt marshes 29. ‘Entanglement’, like physical ‘attachment’ or ‘incorporation’ 37, also increases the local stability of the 2nd habitat-former (Thomsen, unpublished tagging data). I manipulated the amounts of Gracilaria in Zostera marina seagrass beds the East Atlantic (Denmark) at 0.5 and 2 m depth, creating plots in which the 1st habitat former was absent, present at low density, and present at high density. The results from this manipulative experiment supported the hypothesis that the specific amount of the 2nd habitat-former affects habitat cascades for “all invertebrates” (recruits and adults combined), “juvenile recruits”, “gastropods”, and “bivalves”, with more inhabitants associated with the highest added Gracilaria biomass at both depth levels. This experiment also documented that taxonomic richness does not always increase when a 2nd habitat-former is present, probably because this experiment was conducted in a low-diversity system characterized by generalist mobile inhabitants which are likely to be found in most habitats. I also showed that environmental conditions can be essential to document some species-specific habitat cascades. For example, the experiment documented density-dependent positive effects on juvenile sea stars at the deep site, but no effects at the shallow site –where juvenile sea stars were completely absent. This study also indicated that density effects are probably often non-linear. For example, the results indicated impact-thresholds between the low and high added levels of Gracilaria biomass for several inhabitant taxa (though more experimental amount levels are needed to test for density dependent curve-shapes). Finally, the experiment was evaluated in the context of the ADA model 3,13 by discussing how qualitative and quantitative differences in habitat attributes and resource provision between the 1st and 2nd habitat-former likely affected inhabitants with different ecological affinities differently.

Fig 4.1. Experimental at 0.5 m depth in a Zostera marina bed without (left, control), low amounts (centre) and high amounts (right) of the 2nd habitat-forming seaweed, Gracilaria vermiculophylla.

5. Habitat cascades: controlled by the amounts of the secondary habitat-formers – but reciprocal effects can be important; ‘too much’ may ultimately ruin the habitat cascade 38

Our initial research on habitat cascades focused on effects on inhabitants, but overlooked how the 2nd habitat-former affects the 1st HF. Such effects could range from strongly positive to strongly negative depending on (1) the type of association between 1st and 2nd habitat-former (e.g., positive for active incorporation vs. negative for passive entanglement), (2) resource requirements (e.g., plants and animals may facilitate each another but plants and plants compete), (3) the amount of the 2nd habitat-former (the more habitat former present, the stronger the effect) and (4) environmental conditions (e.g., changing from facilitation at stressful conditions to inhibition at benign conditions). Our research has shown support for some of these hypotheses. For example, a meta-analysis of published field experiments confirmed that 2nd habitat-forming seaweeds generally have negative effects on 1st habitat-forming seagrass and that these effects are stronger at high seaweed densities and when the seagrass species is small 38. We have found further support for these findings in a suite of controlled laboratory experiments 39-41. The implication of these results is that (at least in some cases) if the 2nd habitat-former becomes overly abundant, habitat cascades may break down. We here tested this hypothesis by experimentally adding Gracilaria comosa in low and high densities to the very small seagrass species Halophila ovalis in an estuary in the Indian Ocean (Perth, Western Australia) 42. In this field experiment we measured the effects of Gracilaria (2nd habitat-former) on both the seagrass itself (1st habitat-former) and the mobile invertebrate community (inhabitants). We found, as expected, that Gracilaria had negative effects on Halophila, reducing leaf densities by 20 and 40% when exposed to 0.7 and 1.4 kg algal wet weight per m2, respectively. Still, even though this small seagrass was virtually buried by seaweed at the high Gracilaria density, Halophila still survived with >4000 leaves per m2 after one month of seaweed stress. By contrast, invertebrates were positively affected by Gracilaria. The taxonomic richness and densities of dominant crustacean and mollusc species increased with seaweed biomass. More specifically, the abundances of surface-dwelling gastropods, which utilize a two-dimensional habitat, became saturated at low seaweed biomass whereas interstitial isopods and amphipods, which utilize a three-dimensional habitat, continued to increase as seaweed biomass increased. We also found that a non-native habitat-forming snail, the bioturbating Batillaria australis, which itself supports a diverse community of sessile species on its shell 43-45, dominated the surface-dwelling mollusc community. This invasive snail was strongly facilitated by Gracilaria, being 5 times more abundant with seaweeds compared to control plots. Indeed, Batillaria australis was found at densities of >2000 individuals per m2 in high Gracilaria conditions, essentially converting the seagrass bed to a ‘shell-reef’. Finally, we found (as we did in the experiment in Denmark 14) that facilitation from the 2nd habitat-former was only consistent for some juvenile and adults inhabitants (e.g., Batillaria and the infaunal bivalve Soletellina), but not others (e.g., Bedeva and Nassarius snails) 42.


Fig. 5.1. When drift weed (Gracilaria comosa) was added to seagrass beds (composed of the small species Halophila ovalis, Top) in the Swan River Estuary, Western Australia, the non-native invasive snail Batillaria australis colonized in vast numbers (bottom) converting the ‘seagrass bed’ to a ‘mollusc reef’.

6. Habitat cascades can be ‘long’ when more than two habitat-formers co-occur 15

Our early research described habitat cascades founded on only a primary and secondary co-occurring habitat-former. However, as we showed in the Swan River Estuary in Western Australia 42, ecological systems can contain more than two co-occurring habitat-formers. For example, shell-producing molluscs often inhabit the surface of seagrass beds, thereby providing the ‘option’ for seaweeds to either attach to shells or get entangled around seagrass stems and adding another link in the habitat cascade. We therefore conducted an experiment in Denmark, manipulating abundances at 2m depth of both a 1st habitat-former (the seagrass Zostera marina), a 2nd habitat-former (the blue mussel Mytilus edulis that attaches its byssal thread to seagrass leaves), and a 3rd habitat-former (the invasive seaweed Gracilaria vermiculophylla that either entangles around seagrass stems or incorporates into the mussels byssal threads) 15. In this experiment we found a negative effect of Gracilaria on the above-ground biomass of Zostera and a positive effect of Mytilus on the below-ground biomass of Zostera, but no other significant effects between the three habitat-formers 15. Both Mytilus and Gracilaria had positive effects on invertebrate richness and diversity, and Gracilaria also had positive effects on most invertebrate taxa densities. Additional correlation analyses showed that the abundance of invertebrates increased with the biomass of Gracilaria, again demonstrating density-mediated habitat cascades in invaded seagrass beds (see also Thomsen, 2010 14). Gracilaria also modified the multivariate community structure, causing invertebrate communities to be relatively more homogenous. The strong across-the-board facilitation by Gracilaria is not surprising because its coarsely branched fronds provide a complex three-dimensional habitat. This complex habitat which is characterized by different-sized interstitial spaces for different species in different ontogenetic phases to occupy, provides attachment space for bivalves to recruit onto, and likely also protection from predators. By contrast, we found relatively low facilitation from the seagrass on invertebrates, but this may be explained by spill-over effects of removing seagrass leaves in adjacent experimental plots. Furthermore, above-ground removals showed partial recovery causing all plots to have at least some seagrass above-ground biomass. Finally, we did not manipulate below-ground biomass. It is likely that seagrass would have stronger facilitation effects if we instead added Zostera to Mytilus or Gracilaria beds or to un-vegetated sediments. More specifically, we found strong facilitation of herbivorous end-users, like amphipods, isopods and snails, suggesting that species in this trophic level graze on Gracilaria (the 2nd habitat-former) or on associated microscopic epiphytes. Many studies have shown that herbivores can have positive indirect effects on primary habitat-formers by preferentially consuming secondary habitat-formers. This type of ‘keystone consumption’ 3 is thereby a ‘mirror-process’ of cascading habitat-formation/facilitation, but where the former focus top-down inhibition (instead of bottom-up facilitation processes). We noted that our focus was on mobile inhabitants but that facilitation of sessile species using hard substratum for attachment can also be important 3. For example, we also recorded (unpublished data) filamentous brown and red seaweeds attached to Zostera, spirorbid polychaetes attached to Gracilaria, and barnacles, bryozoan and hydrozoa attached to Mytilus, suggesting that these three HF have different sessile communities. In this paper we not only discussed how the ‘Amount’ of the 2nd habitat-former increases facilitation of inhabitants but also how the ecological ‘Differences’ between the habitat-formers can provide unique niche-combinations for different inhabitants with different habitat ‘Affinities’ (the ADA model of Thomsen, 2010. See Appendix 6 in 15 for a tabulated list of ecological differences between the three habitat-formers). We finally suggested that future studies should also test how these invertebrates are facilitated. For example, the inhabitants may benefit from habitat-forming species by escaping enemies (e.g., competitors, parasites, predators) and environmental stress (e.g., waves, heating, desiccation), or by finding friends (e.g., mating partners, mutualist, schooling benefits, Allee effects) and resources (e.g., nesting/resting space or food). These mechanisms will likely differ between environmental conditions (Gracilaria may provide predation refugia in the subtidal zone but ameliorate desiccation stress in the intertidal zone), life histories (a juvenile crab may use Gracilaria to avoid predators whereas the adult crab may use it as feeding ground), and species characteristics (a bivalve may use it as substrate for attachment, whereas a snail may use it for grazing).

Fig. 6.1. Incorporations of Gracilaria (left) and Zostera (right) into Mytilus byssal threads. Incorporation may stabilize the plants, in particular Gracilaria that is only loosely entangled in and around seagrass leaves. However, in the present experiment pegs were used to stabilize Gracilaria and physical facilitation through byssal incorporation did therefore not influence our results.


7. Re-interpretation of another ecological processes as a habitat cascade – and a brief summary of what habitat cascades are 11

In this paper we addressed three issues: (1) that, until the opposite has been demonstrated, hemi-parasites and other 2nd habitat-formers can be considered to be ecologically equivalent, being structurally dependent on primary habitat-formers and typically facilitating inhabitants; (2) that lack of cross-references between marine and aquatic research is unfortunate because both systems are instrumental to conceptual development and testing in ecology, and because many systems are managed across ecosystem-boundaries; and (3) that, because our initial review on habitat and facilitation cascades was detailed and included extensive field data, the more important general take-home messages was likely ‘swamped’.

First, we re-interpreted a fantastic large-scale mistletoe removal experiment 46, that was initially discussed in the context of ‘keystone resource provisioning’ in the simpler context of cascading habitat-formation. We suggested that the more complex explanation, whereby mistletoes transfer nutrients parasitized from a host tree (not measured) to the ground through litter-fall (not measured), facilitating litter-associated invertebrates (not measured) and eventually also facilitating invertebrate-eating birds (measured), could alternatively be interpreted as yet another study documenting that removing secondary habitat-formers results in negative effects on inhabitants. We noted that many aquatic and terrestrial 2nd habitat-formers that are not hemi-parasitic have analogue ecological traits to mistletoes, including negative to neutral effects on their hosts, relatively strong host specificity, high litter production and strong influence on nutrient and biogeochemical cycling. This re-interpretation allowed us to calculate a simple standardized effect size (magnification ratio) that can be compared across studies, scales and ecosystems 3. From this standardization procedure we showed that the mistletoe removal experiment stood out from the previous published habitat cascade experiments by its unusual large sample grain (100,000 m2) and spatial extent (1,600,000,000 m2), that were dramatically larger than any published habitat cascade experiment (online Table S1 in 11). However, the magnification ratios and the size-ratio between the 2nd to 1st habitat-former was not unusual for the mistletoe removal study.

Fig. 7.1. 1st habitat-formers cause indirect positive effects on inhabitants by physically controlling 2nd habitat-formers. Example 1: A eucalyptus tree provides habitat for birds and mistletoes, and mistletoes provide additional habitat for additional birds (i.e., the tree has both direct and indirect positive effects on birds). Examples 2-17: Examples of co-existing habitat-formers in terrestrial (2-5), semi-terrestrial (6-8), freshwater (9, 13), and marine (10-17) ecosystems (cf. online supplement in Thomsen & Wernberg 2014 for details about these habitat-formers, inhabitants and relevant scientific case-studies). Note to example 9; these small epiphytes are not habitat-formers sensu strictu but more like a trophic subsidy; i.e., this example also show that consumers can have positive indirect effects on 1st habitat-formers by preferentially consuming 2nd ‘habitat modifiers’. This type of ‘keystone consumption’ is thereby a ‘mirror-process’ to cascading habitat-formation and modification.

Second, we highlighted that most studies that we could re-interpret as habitat cascade experiments were focused on terrestrial epiphytes and mistletoes and did not cite aquatic case studies. We then argued that lack of cross-references to aquatic case studies is unfortunate because aquatic systems often have been instrumental to conceptual development and testing in ecology, and also because managers often have to manage systems across ecosystems. We noted that most conservation research to date has focused on more obvious effects associated with the direct loss of 1st habitat-formers. However, neglecting how associated 2nd habitat-formers affect productivity, biodiversity and ecosystem functioning could underestimate the loss of ecosystem services associated with the continued degradation of natural ecosystems, and make it more difficult to predict, prevent or ameliorate the loss of 1st habitat-formers.

Finally, we wrote a brief summary to highlight key issues discussed in length in 3. Here, we (again) argued that the magnitude of facilitation associated with the 2nd habitat-former is great (1) when the 2nd habitat-former is larger, more abundant and more ecologically/functionally different than the 1st habitat-former, (2) at opposite end-points of environmental stress gradients where inhabitants are more likely to escape stress and enemies and find resources and friends, and (3) when alternative pathways for inhabitants to escape stress and enemies and find resources and friends, are weak (= weak dilution/strong concentration-processes), for example if spatio-temporal heterogeneity, food web complexity, or adjacent and interspersed habitats are low and small. Thus, cascading habitat-formation is typically density-mediated (however, trait-mediated indirect facilitation can also occur). We also exemplified how facilitation of inhabitants can occur autogenically (i.e., within/on the 2nd habitat-former) and allogenically ( i.e., through ecological subsidy) from either local (e.g., mistletoe litter fallen to the forest floor) or from adjacent ecosystems (e.g., through advection processes, such as when seaweeds fixed in polychaete gardens dislodge and are transported to adjacent salt marshes together with their end-user communities).

Fig. 7.2. Cascading habitat-formation (A) can sometimes be interpreted as a ‘mirror process’ of keystone consumption (B), see also example 9 in Fig. 7.1)

8. Habitat cascades also occur in rocky intertidal systems – and can be controlled by ‘obligate’ 2nd habitat-formers 13

Few studies have quantified habitat cascades from rocky intertidal systems, across ecological transition zones, or where the 2nd H habitat-former is an obligate species that only can be found on a single species of 1st habitat-former. We conducted research on the intertidal rocky platforms of Kaikoura, New Zealand to address these research gaps 13. We first quantified distributions of the seaweed Hormosira banksii (1st habitat-former) and its obligate epiphyte Notheia anomala (2nd habitat-former) at different tidal elevations in summer and winter. This analysis showed that the 1st and 2nd habitat-formers were, in both seasons, most abundant at ‘high’ and ‘low’ tidal elevations respectively, probably driven by contrasting responses to competitors and desiccation. We subsequently quantified taxonomic richness and abundances of mobile invertebrate inhabitants associated with Hormosira and various levels of epiphytic Notheia. Hormosira fronds were collected from different elevations, seasons, diurnal cycles, with different neighbouring algae and following an epiphyte-removal experiment. All tests from both the ‘mensurative’ (surveys) and manipulative experiments showed, like much of our previous research 3,15,42, positive density-dependent effects of the 2nd habitat-former on both taxonomic richness and abundances of the inhabitants, with strongest facilitation occurring at the transition from intertidal to subtidal habitats. Effects varied based on the presence and identity of neighboring seaweeds. Interestingly, density effects were stronger for Notheia than Hormosira (the latter of which has been shown to be a direct driver of diversity patterns), even though biomass was one order of magnitude larger for Hormosira. Perhaps the finer structure and smaller interstitial spaces from Notheia provide a superior habitat for many small inhabitants compared with the coarser Hormosira fronds. On the basis of these results, and as hypothesised in 3, we suggested that habitat cascades become increasingly important when (1) there is more of the secondary habitat-former (= amount, e.g., its size, abundance, longevity), (2) the secondary habitat-former is form–functionally different, and (3) clients have high host-specificity (= affinity) for the secondary habitat-former. We suggested that whereas the ‘more habitat’ model should increase both diversity and abundances of inhabitants, combining ‘different habitat’ and ‘habitat-affinity’ explanatory models could potentially affect diversity more than abundances (because the combined two models represent the match between new and different empty niches and new clients with novel traits that can fill these niches). To use an extreme example: aquatic invertebrates inhabiting bromeliad phytotelmata on host trees increase richness dramatically but barely affect total abundances of the client pool that inhabit the combined epiphyte–host tree complex (see 13 for this example). Interestingly, we also found several Notheia fronds that were heavily epiphytised by red filamentous algae, thereby potentially facilitating more and different inhabitants through higher-order long habitat cascades. Our focus was simply to quantify the existence of a particular habitat cascade on general biodiversity responses. It is still unclear whether the inhabitants we observed mainly use Notheia to avoid enemies, to avoid stress, to find facilitators, to find resources or, more likely, a combination of these general mechanisms 11. We also noted that because Notheia is an obligate 2nd habitat-former, any anthropogenic threat to Hormosira is likely to have a strong indirect cascading negative effect on invertebrate clients, as host switching by Notheia is simply not possible. We finally suggested that habitat cascades likely are common in marine benthic systems where ‘epibiosis’ often is a dominant life form.

Fig. 8.1. Diagram outlining the rocky intertidal HormosiraNotheia–invertebrate habitat cascade. The primary habitat-former, Hormosira, (a) has indirect positive effects (bend arrow) on small invertebrate clients like snails, amphipods and copepods (c) by providing structural support to the secondary habitat-former, Notheia (b). More taxa and individuals inhabited Notheia than Hormosira per gram dry weight biomass, documenting that Notheia increases the likelihood of inhabitants to find facilitators and resources and avoid enemies and stress.

9. Long habitat cascades as colonization events or networks with loops and feedbacks 47

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. In this paper we quantified 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 in a loop, 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, and accumulated shell biomass, but less with the size of individual shells. 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. More specifically, different inhabitants had varied abundances on different co-occurring habitat-formers. These differences are not only explained by the amount of available habitat (‘amount’), but could also depend on the compatibility of traits between inhabitants and habitat-formers. For example, trochid snails were abundant on seaweeds, probably because they are mobile grazers searching for food. Alternatively, trochids may inhabit seaweeds to avoid predation and environmental stressors such as desiccation and temperature fluctuations. Sessile invertebrate inhabitants such as Conopeum can also select for certain substrates, but only at settlement, whereas for the seaweeds, settlement is more likely a passive propagule rain. Differences in affinities between inhabitants could reflect both pre-settlement processes like early microbial inhibition, post-settlement processes like competition for space and trophic interactions, or physiological and biomechanical stress limitations.

Finally, manipulative experiments confirmed that the amount of seaweed and trochids were important and consistent regulators of the habitat cascade in different estuarine environments (i.e., in different locations, experimental durations and habitats). We interpreted this long cascade both as (a) a static ‘habitat-formation network’ that describes the likelihood of an inhabitant being found attached to a specific habitat-former and (b) a temporal succession of events starting with the recruitment of the mollusc Austrovenus, the shells of which are colonized by other habitat-formers over time. We concluded, in support of the ADA-model, 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.

Fig. 9.1. A sixth-level long habitat cascade in the Avon-Heathcote Estuary, New Zealand portrayed as (a) a static habitat-formation interaction network and (b), a succession of colonization events. a. The direction and thickness of arrows reflect the ‘total affinity’ of inhabitants for habitat-formers (the number next to the ‘attachment arrow head’ = ‘Total Affinity’ = number of attached inhabitants per gram dry weight habitat-former, see Table 1 for calculations). ‘Rare’ and ‘Never?’ (dotted lines) represents plausible qualitative affinities that will require more sample-intensive surveys to enumerate. Austrovenus cannot physically attach to organisms and has therefore no attachment arrows. b. 1. Juvenile Austrovenus colonize a mudflat, 2. Austrovenus grows into a larger and older 1st order habitat-former. 3. Shell protrudes above the sediment surface and Ulva attaches. 4. Ulva grows into a large 2nd order habitat-former that is colonized by trochids. 5. Close-up of 3rd order habitat-forming trochid colonized by Conopeum (and Ulva), 6. The 4th order habitat-former Conopeum is colonized by the 5th order habitat-forming Gigartina (and Ulva) which, again, in a loop, is colonized by trochids.


Other ways to communicate about habitat cascades

Our group is also promoting research on habitat and facilitation cascades through



1              Altieri, A. H., Silliman, B. R. & Bertness, M. D. Hierarchical organization via a facilitation cascade in intertidal cordgrass bed communities. The American Naturalist 169, 195-206 (2007).

2              Mouritsen, K. N. Intertidal facilitation and indirect effects: causes and consequences of crawling in the New Zealand cockle. Mar. Ecol. Prog. Ser. 271, 207-220 (2004).

3              Thomsen, M. S. et al. Habitat cascades: The conceptual context and global relevance of facilitation cascades via habitat formation and modification. Integrative and Comparative Biology 50, 158-175 (2010).

4              Angelini, C. & Silliman, B. R. Secondary foundation species as drivers of trophic and functional diversity: evidence from a tree-epiphyte system. Ecology 95, 185-196 (2014).

5              Thomsen, M. S. & McGlathery, K. Facilitation of macroalgae by the sedimentary tube forming polychaete Diopatra cuprea. Estuarine Coastal and Shelf Science 62, 63-73 (2005).

6              Gribben, P. E. et al. Behavioural interactions between ecosystem engineers control community species richness. Ecology Letters 12, 1127-1136 (2009).

7              Angelini, C., Altieri, A. H., Silliman, B. R. & Bertness, M. D. Interactions among foundation species and their consequences for community organization, biodiversity, and conservation. BioScience 61, 782-789 (2011).

8              Wahl, M. Epibiosis Ecology, Effects and Defences Ecological Studies, Marine Hard Bottom Communities, Part 1 206, 61-72 (2009).

9              Stevens, G. C. Lianas as structural parasites: the Bursera simaruba example. Ecology 68, 77-81 (1987).

10           Gutiérrez, J. L. & Palomo, M. G. Increased algal fouling on mussels with barnacle epibionts: a fouling cascade. Journal of Sea Research 112, 49-54 (2016).

11           Thomsen, M. S. & Wernberg, T. On the generality of cascading habitat-formation. Proceedings of the Royal Society B: Biological Sciences 281(1777):20131994 (2014).

12           Fernandez-Leborans, G. Protist-bryozoan-crustacean hyperepibiosis on Goneplax rhomboides (Linnaeus, 1758) (Decapoda, Brachyura) from the NW Mediterranean coast. Crustaceana 76, 479-497 (2003).

13           Thomsen, M. S., Metcalfe, I., South, P. & Schiel, D. R. A host-specific habitat former controls biodiversity across ecological transitions in a rocky intertidal facilitation cascade. Marine and Freshwater Research 67, 144-152 (2016).

14           Thomsen, M. S. Experimental evidence for positive effects of invasive seaweed on native invertebrates via habitat-formation in a seagrass bed. Aquatic Invasions 5, 341-346 (2010).

15           Thomsen, M. S., Staehr, P. A., Nejrup, L. & Schiel, D. R. Effects of the invasive macroalgae Gracilaria vermiculophylla on two co-occurring foundation species and associated invertebrates. Aquatic Invasions 8, 133-145 (2013).

16           Cruz-Angon, A., Baena, M. L. & Greenberg, R. The contribution of epiphytes to the abundance and species richness of canopy insects in a Mexican coffee plantation. Journal of Tropical Ecology 45, 453–463 (2009).

17           Bergsma, G. S. Coral mutualists enhance fish abundance and diversity through a morphology-mediated facilitation cascade. Marine Ecology Progress Series 451, 151-161, doi:10.3354/meps09615 (2012).

18           Bishop, M. J., Byers, J. E., Marcek, B. J. & Gribben, P. E. Density-dependent facilitation cascades determine epifaunal community structure in temperate Australian mangroves. Ecology 93, 1388-1401 (2012).

19           Jones, C. G., Lawton, J. H. & Shachak, M. Organisms as ecosystem engineers. Oikos 69, 373-386 (1994).

20           Dayton, P. K. Competition, disturbance, and community organization: the provision and subsequent utilization of space in a rocky intertidal community. Ecological Monographs 43, 353-389 (1971).

21           Huston, M. A. Biological diversity: the coexistence of species on changing landscapes. Cambridge University Press, 681 (1994).

22           Warming, E. Plantesamfund. Grundtrak af den økologiske plantegeografi. (Philipsen, Copenhagen, 1895).

23           Bruno, J. F. & Bertness, M. D. 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 (2001).

24           Wright, J. T. & Jones, C. G. The concept of organisms as ecosystem engineers ten years on: progress, limitations, and challenges. BioScience 56, 203-209 (2006).

25           Ellison, A. M. et al. Loss of foundation species: consequences for the structure and dynamics of forested ecosystems. Frontiers in Ecology and Environment 3, 479-486 (2005).

26           Thomsen, M. S. Macroalgal distribution patterns and ecological performances in a tidal coastal lagoon, with emphasis on the non-indigenous Codium fragile ssp. tomentosoides, (2004).

27           Thomsen, M. S., McGlathery, K. J. & Tyler, A. C. Macroalgal distribution patterns in a shallow, soft-bottom lagoon, with emphasis on the nonnative Gracilaria vermiculophylla and Coldium fragile. Estuaries and Coasts 29, 465-473 (2006).

28           Nyberg, C. D., Thomsen, M. S. & Wallentinus, I. Flora and fauna associated with the introduced red alga Gracilaria vermiculophylla. European Journal of Phycology 44, 395-403, doi:10.1080/09670260802592808 (2009).

29           Thomsen, M. S., McGlathery, K. J., Schwarzschild, A. & Silliman, B. R. Distribution and ecological role of the non-native macroalga Gracilaria vermiculophylla in Virginia salt marshes. Biological Invasions 11, 2303-2316, doi:10.1007/s10530-008-9417-9 (2009).

30           Rodriguez, L. F. Can invasive species facilitate native species? Evidence of how, when, and why these impacts occur. Biological Invasions 8, 927-939 (2006).

31           Brooker, R. W. & Callaway, R. M. Facilitation in the conceptual melting pot. Journal of Ecology 97, 1117-1120 (2009).

32           Bertness, M. & Callaway, R. Positive interactions in communities. TRENDS in Ecology and Evolution 9, 191-193 (1994).

33           Stachowicz, J. J. Mutualism, facilitation, and the structure of ecological communities. BioScience 51, 235-246 (2001).

34           Soliveres, S. et al. Microhabitat amelioration and reduced competition among understorey plants as drivers of facilitation across environmental gradients: Towards a unifying framework. Perspectives in Plant Ecology, Evolution and Systematics 13, 247-258 (2011).

35           Boulant, N., Navas, M.-L., Corcket, E. & Lepart, J. Habitat amelioration and associational defence as main facilitative mechanisms in Mediterranean grasslands grazed by domestic livestock. Ecoscience 15, 407-415 (2008).

36           Thomsen, M. S. et al. Gracilaria vermiculophylla in northern Europe, with focus on Denmark, and what to expect in the future. Aquatic Invasions 2, 83-94 (2007).

37           Thomsen, M. S. Species, thallus size and substrate determine macroalgal break force and break location in a low-energy soft-bottom lagoon. Aquatic Botany 80, 153-161, doi:10.1016/j.aquabot.2004.08.002 (2004).

38           Thomsen, M. S. et al. A meta-analysis of seaweed impacts on seagrasses: generalities and knowledge gaps. PLOS one 7, e28595 (2012).

39           Hoeffle, H., Thomsen, M. S. & Holmer, M. High mortality of Zostera marina under high temperature regimes but minor effects of the invasive macroalgae Gracilaria vermiculophylla. Estuarine, Coastal and Shelf Science 92, 35-46 (2011).

40           Hoeffle, H., Wernberg, T., Thomsen, M. S. & Holmer, M. Drift algae, an invasive snail and elevated temperature reduces the ecological performance of a warm-temperate seagrass via additive effects. Marine Ecology Progress Series 450, 67-80, doi:10.3354/meps09552 (2012).

41           Holmer, M., Wirachwong, P. & Thomsen, M. S. Negative effects of stress-resistant drift algae and high temperature on a small ephemeral seagrass species. Marine Biology 158, 297-309 (2011).

42           Thomsen, M. S., de Bettignies, T., Wernberg, T., Holmer, M. & Debeuf, B. Harmful algae are not harmful to everyone. Harmful Algae 16, 74-80 (2012).

43           Thyrring, J., Thomsen, M. S., Brunbjerg, A. K. & Wernberg, T. Diversity and abundance of epibiota on invasive and native estuarine gastropods depend on substratum and salinity. Marine and Freshwater Research 66, 1191–1200 (2015).

44           Thyrring, J., Thomsen, M. & Wernberg, T. Large-scale facilitation of a sessile community by an invasive habitat-forming snail. Helgoland Marine Research 67, 789-794, doi:10.1007/s10152-013-0363-2 (2013).

45           Thomsen, M. S., Wernberg, T., Tuya, F. & Silliman, B. R. Ecological performance and possible origin of a ubiquitous but under-studied gastropod. Estuarine Coastal and Shelf Science 87, 501-509 (2010).

46           Watson, D. M. & Herring, M. Mistletoe as a keystone resource: an experimental test. Proceedings of the Royal Society B: Biological Sciences 279, 3853-3860 (2012).

47           Thomsen, M. et al. A sixth-level habitat cascade increases biodiversity in an intertidal estuary. Ecology and Evolution 6, 8291–8303 (2016).