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Aug 29, 2011 - Ecologically Informed Engineering Reduces Loss of Intertidal Biodiversity on Artificial Shorelines. Mark A. Browne*†‡ and M. Gee Ch...
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Ecologically Informed Engineering Reduces Loss of Intertidal Biodiversity on Artificial Shorelines Mark A. Browne*,†,‡ and M. Gee Chapman† † ‡

Centre for Research on Ecological Impacts of Coastal Cities, School of Biological Sciences, University of Sydney, NSW 2006, Australia School of Biology & Environmental Science, University College Dublin, Dublin, Ireland

bS Supporting Information ABSTRACT: Worldwide responses to urbanization, expanding populations and climatic change mean biodiverse habitats are replaced with expensive, but necessary infrastructure. Coastal cities support vast expanses of buildings and roads along the coast or on “reclaimed” land, leading to “armouring” of shorelines with walls, revetments and offshore structures to reduce erosion and flooding. Currently infrastructure is designed to meet engineering and financial criteria, without considering its value as habitat, despite artificial shorelines causing loss of intertidal species and altering ecological natural processes that sustain natural biodiversity. Most research on ameliorating these impacts focus on soft-sediment habitats and larger flora (e.g., restoring marshes, encouraging plants to grow on walls). In response to needs for greater collaboration between ecologists and engineers to create infrastructure to better support biodiversity, we show how such collaborations lead to small-scale and inexpensive ecologically informed engineering which reduces loss of species of algae and animals from rocky shores replaced by walls. Adding experimental novel habitats to walls mimicking rock-pools (e.g., cavities, attaching flowerpots) increased numbers of species by 110% within months, in particular mobile animals most affected by replacing natural shores with walls. These advances provide new insights about melding engineering and ecological knowledge to sustain biodiversity in cities.

’ INTRODUCTION Urbanization has transformed the earth’s surface and urban infrastructure—housing, utilities, transportation and commerce— have replaced natural habitats over large areas. These transformed landscapes typically support fewer species, although some species reach pest proportions. In addition, species found in cities tend to be homogenized, with similar species found in cities worldwide.1 Coastal infrastructure, often called coastal “armouring”,2 is built along natural shorelines or on “reclaimed” land to protect infrastructure from waves and erosion. It is getting taller and spreading3 and with increasing urbanization, rising sealevels and more stormy weather predicted, is set to increase. In parts of Japan,4 U.S.,2 Europe,5 and Australia,6 more than half of the coastline has been replaced by artificial structures. The most extensive type of coastal “armouring” is revetments and seawalls, which may be the only “rocky” habitat for kilometres in major ports and estuaries in and around cities (Figure 1a). Although there have been many attempts to restore degraded intertidal habitats around cities, for example, marshes,7 mangroves,8 and beaches,9 rocky shores have been considered resilient to such change because many visually dominant species appear to thrive on artificial habitats.10 Closer study has revealed, however, that many intertidal species, particularly larger mobile animals such as starfish, urchins, and large gastropods, do not live on seawalls,11,12 whereas those that do may be genetically less diverse,13 grow or reproduce slowly,14 or change their intra- or interspecific interactions,1517 particularly when structures are colonized by invasive species.18 Thus expanding urbanization has r 2011 American Chemical Society

potentially serious implications for intertidal assemblages from rocky shores, a problem that is only recently been recognized.18,19 The value of “armoured” shores as ecological habitat in urban areas has mostly been investigated with respect to plants and fish. Thus, Francis and Hoggart20 showed more than three times as many plants living on walls on the River Thames in central London than on intertidal foreshores and the habitat in and around piers and docks support large diversities of fish.21,22 Numerous programmes of restoration involve the addition of “natural” habitat offshore from “armoured” shores,23 both to decrease impacts on the shoreline itself and to add habitat such as oyster reef, vegetation, or saltmarshes to bare sediments. There have, however, been few attempts to change the quality of the habitat provided by the walls themselves for species that live on them, even though walls may be valuable habitat for species whose natural rocky habitat may be lost to infrastructure, or disturbed by other human activities.19,24 In addition, many such experiments have been small-scale, addressing focused problems. Ecological-engineering2529 - melding engineering criteria and ecological knowledge to create better urban environments has revolutionized modern building. Growing plants on walls and roofs of buildings can improve aesthetics, produce crops, remove air-borne toxicants or cools cities.28 Natural marshes can Received: June 6, 2011 Accepted: August 29, 2011 Revised: August 27, 2011 Published: August 29, 2011 8204

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Environmental Science & Technology

Figure 1. (A) Port of Vancouver (Canada) illustrating the extent of artificial shorelines composed of featureless seawalls. (B) Flower pots creating novel habitat on seawalls in Sydney Harbour (Australia). (C) Total number of taxa unique to wall fac-ades (black), unique to flower pots (white) and shared (gray) at midshore levels; data summarized over two sites and seven months, using published methods.17 (D) Pots provided habitat for many algae (e.g., turf-forming red algae such as Corallina officinalis - i), sessile animals, such as ascidians, filter-feeding tubeworms and sponges, and mobile animals, such as omnivorous crabs (e.g., Leptograpsus variegates - ii), grazing starfish (e.g., Patiriella exigua - iii), grazing amphipods and many gastropods (e.g., Austrocochlea concamerata - iv, Alaba opiniosa - vi).

clean wastewater better than do treatment works.29 To date, despite the cogent argument that walls are underused habitats in cities and that relatively cheap and easy engineering can improve their value as habitat for many plants and animals,19,30 there has been relatively little application of the concept of ecologicalengineering to the design of coastal “armouring” in order to increase local levels of biodiversity.30 This is particularly so for intertidal marine animals and seaweeds.19

’ EXPERIMENTAL MODIFICATIONS OF SEAWALLS IN SYDNEY HARBOUR Here we describe an extensive set of experiments in Australia investigating adding novel habitats to intertidal seawalls to create better environments for intertidal species. These experiments all involved close collaborations between ecologists and engineers building or repairing seawalls, who were very responsive to the needs of replication and good experimental design. The earlier experiments have been described in detail elsewhere. The original experiments added new habitats to walls at a small-scale

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because of concern by authorities that adding larger habitats to seawalls would alter their aesthetic value.20 These experiments included adding holes and crevices in the fac-ades of the blocks making up the wall19 and indenting the mortar between blocks to create narrow crevices.19,31 Although successful in enhancing the number of species living on the walls in the short term, longer term they were less successful as they filled with sessile animals, so the available habitat was lost. These were followed by attempts to create larger cavities in the vertical fac-ades of walls. These cavities retain water during lowtide and, thus, imitate rock-pools, although unlike natural pools they are always shaded by the wall. First, they were created by using sand-bags as bloks of masonry during repair of existing walls.19 When removed, they created hollows in the wall that were colonized by nudibranchs, octopuses and urchins, species that generally cannot live on vertical intertidal walls. A much larger experiment on a newly built wall omitted masonry-blocks, leaving cavities in the walls, to which small-lips were added to create enclosed pools.32 This was a large-scale experiment, with replicate “pools” created at three heights in each of three replicate sites. After a year, these had increased the number of species living on the walls, particularly midshore, with 57% more species of algae and 42% more species of sessile animals. Such approaches are cheap and easy, requiring no additional material, but require the cooopration of the engineers building walls to supervise changes in plans. They can, however, only be used when building walls out of blocks of material. Adding similar microhabitat into concrete or existing walls is not usually feasible. So, inspired by the concept of “living walls”,27,29 concrete flower pots were used to mimic rock-pools. Flower pots have been used for thousands of years to grow plants in novel locations and inhospitable habitats. Here, they also prove to be a tractable method for ecologically engineering seawalls to increase intertidal biodiversity. Concrete pots, built to withstand wave-action, were attached at mid- and highshore tidal levels (1.01.3 m 1.61.9 m above chart datum, respectively) to seawalls at Cremorne Point (33° 500 50.3298S; 151° 130 49.0578E) and Careening Cove (33° 500 42.7194S, 151° 130 6.1464E) in Sydney Harbour in December, 2009, with six replicate pots at each height in each site. These more resembled natural pools than did the earlier engineered habitats in that they created pools of water during low tide that were exposed to the sun, rather than continually shaded and they were flushed by the tide each high tide. Two sizes of pots (10 and 6 L) were used; these had the same diameter (360 mm) but different depths (380 and 220 mm respectively). All animals and plants found in the pots and plots on the walls were counted weekly for 6 weeks, then at monthly and 3 monthly intervals. After 7 months there were still clear differences in the assemblages living in pots and on walls so further sampling was not required. Some pots were lost due to wave action, so here we describe colonization of animals and plants into 10 L pots at the midshore level at both sites after 7 months. Square plots of similar area to the internal surface area of the 10 L pots (2500 cm2) were randomly interspersed among the pots on the fac-ade of the wall for comparsison with the assemblage living on the wall. It was not possible to clear the assemblage living on the wall due to restrictions by the authorities, so the existing assemblage was mature, as described by Chapman and Bulleri6 for other seawalls in the harbor. It was comprised of large amounts of bare space (>70%) with some barnacles, mussels (Mytilus sp.), oysters (Saccostrea glomerata), and brown (Ralfsia verrucosa, Endarachne binghamiae), and red 8205

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Environmental Science & Technology algae (Hildenbrandia rubra, Gelidium pusillum). The experiment thus examined what additional species would be added to a mature “wall assemblage” (the wall was many decades old and was unlikely to have been cleaned in that time) by the addition of pots, rather than comparing colonization of the pots and the bare wall. Using a similar approach to Chapman & Blockley,32 the taxa were divided into three groups: those found (i) only on the walls, (ii) only in pots, and (iii) in both habitats. This allowed us to test the prediction that species living in rock-pools on natural shores, but not generally on seawalls, would be found in these pots, but not in the uncleared surrounding plots. By 7 months, 25 species had colonized the pools which were not found in the assemblage on the walls (an increase of 64%). These included algae (50% more species), sessile animals (39% more) and mobile animals (118% more; Figure 1bd, Supporting Information Table S1). The taxa unique to the pots were diverse, including red (e.g., Polysiphonia sp.) and green algae (e.g., Ulva lactuca, Bryposis sp.) and many sessile animals, such as ascidians (e.g., Pyura stolonifera), sponges (e.g., Haliclona sp.) and tubeworms (e.g., Galeolaria caespitosa, Hydroides sp.). Although many sessile animals live on seawalls, soft-bodied sponges, ascidians and branching bryozoans seldom do so at midshore levels unless protected in deep crevices. Similarly, these species are largely confined to rock-pools at midshore levels of rocky shores. More importantly, this assemblage included many mobile animals, such as grazing snails (e.g., Littorina unifasciata, Nodilittorina pyramidalis, Austrocochlea porcata, Austrocochlea concamerata, Alaba opiniosa), limpets (e.g., Patelloida alticostata, P. mufria, Kerguelenela lateralis), amphipods (e.g., Caprellids), and starfish (e.g., Patiriella exigua), and crabs (e.g., Leptograpsus variegatus). Many of these species are not found on unmodified intertidal seawalls6 and thus are most threated by replacement of natural shores by walls.

’ WHERE TO FROM HERE As cities grow more habitat will be lost as infrastructure spreads. Although restoration is an important tool for conservation,3335 it is unlikely to be an option once natural habitats have been replaced by expensive infrastructure. It has been estimated that it will cost £590 billion to protect the world’s coastal cities from rising sea-levels and increases in storms36 and 2097% of this will be spent building new seawalls or increasing the stability, height and length of existing walls.3,36 Our work shows that collaboration between experimental ecologists and engineers during the process of designing and building this infrastructure, as promulgated by Francis and Hoggart,20 can lead to a range of cheap and easy engineering techniques that can be applied to new and existing coastal infrastructure. For instance adding cavities into seawalls was actually cheaper than building a seawall without them because fewer expensive sandstone blocks were used, whereas the cost of a flower pot, without a metal bracket and fixings is less than AUS$200 each. Work is now needed to determine how durable the flower pots and their fixings are over longer periods, but they do seem to be a useful approach to try to sustain, rather than erode, levels of intertidal biodiversity in and around cities. ’ ASSOCIATED CONTENT

bS

Supporting Information. Table S1. This material is available free of charge via the Internet at http://pubs.acs.org.

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’ AUTHOR INFORMATION Corresponding Author

*Phone: +353 (0) 870 916 484; fax: +353 (0) 1 716 1152; e-mail: [email protected].

’ ACKNOWLEDGMENT We thank North Sydney Council, Woollahra Municipal Council and the City of Sydney for support and access to study sites. J. Thompson of John Nixon Engineering Pty Ltd and MacLeod Consultants were particularly helpful in many of these experiments. A. Luck, B. Panayotakos, G. Deavin, C. Myers, M. Day, J. Sidie, B. Twist, J. Commins, D. Beechey are thanked for assistance and photographs. The Centre for Research on Ecological Impacts of Coastal Cities (University of Sydney), ECS Services, Antique Stone and various local government authorities provided support for this research. Manuscript was improved by comments from S. J. Simpson, R. Shine, A. J. Underwood and three anonymous referees. ’ REFERENCES (1) Mckinney, M. L., Lockwood, J. L. Biotic homogenization: a few winners replacing many losers in the next mass extinction. Trends Ecol. Evol. 1999, 14, 450-453; DOI 10.1016/S0169-5347(99)01679-1 (2) Davis, J. L. D., Levin, L. A., Walther, S. M. Artificial armoured shorelines: sites for open-coast species in a southern California bay. Mar. Biol. 2002, 140, 12491262; DOI 10.1007/s00227-002-0779-8 (3) IPCC. Climate Change 2007: Impacts, Adaptation and Vulnerability. Contribution of Working Group II to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change, Chapter 6; Cambridge University Press: Camrbidge, 2007). (4) Koike, K. The countermeasures against coastal hazards in Japan. Geojournal 1996, 38, 301312; DOI: 10.1016/j.coastaleng.2005.09.007 (5) Airoldi, L., Abbiati, M. Beck, M. W., Hawkins, S. J. Jonsson, P. R., Martin, D., Moschella, P. S., Sundelo, A., Thompson, R. C., Aberg, P. An ecological perspective on the deployment and design of low crested and other hard coastal defence structures. Coast. Eng. 2005, 52, 10731087; DOI: 10.1016/j.coastaleng.2005.09.007 (6) Chapman, M. G., Bulleri, F. Intertidal seawalls  new features of landscape in intertidal environments. Landscape Urban Plan. 2003, 62, 159172; DOI: 10.1016/S0169-2046(02)00148-2 (7) Zedler, J. B., Callaway, J. C., Sullivan, G. Declining biodiversity: Why species matter and how their functions might be restored in Californian tidal marshes. BioScience 2001, 51, 1005-1017; DOI: 10.1641/0006-3568(2001)051[1005:DBWSMA]2.0.CO;2 (8) Alongi, D. M. Present state and future of the world’s mangrove forests. Environ. Conserv. 2002, 29, 331-349; DOI: 10.1017/S0376892902000231 (9) Nordstrom, K. F. Beach nourishment and coastal habitats: Research needs to improve compatibility. Restor. Ecol. 2005, 13, 215222; DOI: 10.1111/j.1526-100X.2005.00026.x (10) Thompson, R. C., Crowe, T. P., Hawkins, S. J. Rocky intertidal communities: past environmental changes, present status and predictions for the next 25 years. Environ. Conserv. 2002, 29, 168-191; DOI: 10.1017/S0376892902000115 (11) Chapman, M. G. Paucity of mobile species on constructed seawalls: effects of urbanization on biodiversity. Mar. Ecol.: Prog. Ser. 2003, 264, 21-29; DOI: 10.3354/meps264021 (12) Bulleri, F., Chapman, M. G. The introduction of coastal infrastructure as a driver of change in marine environments. J. Appl. Ecol. 2010, 47, 2635; DOI: 10.1111/j.1365-2664.2009.01751.x (13) Fauvelot, C., Bertozzi, F., Costantini, F., Airoldi, L. Abbiati, M. Lower genetic diversity in the limpet Patella caerulea on urban coastal structures compared to natural rocky habitats. Mar. Biol. 2009, 156, 2313-2323; DOI: 10.1007/s00227-009-1259-1 8206

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