Journal of Applied Ecology 2010, 47, 1119–1127
doi: 10.1111/j.1365-2664.2010.01852.x
Testing alternate ecological approaches to seagrass rehabilitation: links to life-history traits Andrew D. Irving*, Jason E. Tanner, Stephanie Seddon, David Miller†, Greg J. Collings, Rachel J. Wear, Sonja L. Hoare and Mandee J. Theil South Australian Research and Development Institute (Aquatic Sciences), PO Box 120, Henley Beach, SA 5022, Australia
Summary 1. Natural resources and ecosystem services provided by the world’s major biomes are increasingly threatened by anthropogenic impacts. Rehabilitation is a common approach to recreating and maintaining habitats, but limitations to the success of traditional techniques necessitate new approaches. 2. Almost one-third of the world’s productive seagrass meadows have been lost in the past 130 years. Using a combined total of three seagrass species at seven sites over 8 years, we experimentally assessed the performance of multiple rehabilitation methods that utilize fundamentally different ecological approaches. 3. First, traditional methods of transplantation were tested and produced varied survival (0–80%) that was site dependent. Secondly, seedling culture and outplanting produced poor survival (2–9%) but reasonable growth. Finally, a novel method that used sand-filled bags of hessian to overcome limitations of traditional techniques by facilitating recruitment and establishment of seedlings in situ produced recruit densities of 150–350 seedlings m)2, with long-term survival (up to 38 months) ranging from 0 to 72 individuals m)2. 4. Results indicate that facilitating seagrass recruitment in situ using hessian bags can provide a new tool to alleviate current limitations to successful rehabilitation (e.g. mobile sediments, investment of time and resources), leading to more successful management and mitigation of contemporary losses. Hessian bags have distinct environmental and economic advantages over other methods tested in that they do not damage existing meadows, are biodegradable, quick to deploy, and cost less per hectare (US$16 737) than the estimated ecosystem value of seagrass meadows (US$27 039 year)1). 5. Synthesis and applications. This research demonstrates how exploring alternate ecological approaches to habitat rehabilitation can expand our collective toolbox for successfully re-creating complex and productive ecosystems, and alleviate the destructive side-effects and low success rates of more traditional techniques. Moreover, new methods can offer economic and environmental solutions to the restrictions placed upon managers of natural resources. Key-words: Amphibolis antarctica, hessian, recruitment, restoration, seedling, transplant
Introduction Optimally functioning habitats and ecosystems maintain the Earth’s biosphere and human welfare, but many face impacts *Correspondence author. Southern Seas Ecology Laboratories, DX 650 418, School of Earth and Environmental Sciences, University of Adelaide, Adelaide, SA 5005, Australia. E-mail:
[email protected] †Present address: Coast & Marine Conservation Branch, Department of Environment and Natural Resources, Keswick, SA 5035, Australia
from an increasing number of anthropogenic threats (Vitousek et al. 1997; Bellwood et al. 2004). Such impacts jeopardize the global value of environmental, economic, and social benefits provided by the world’s major biomes, which have collectively been estimated at US$46 trillion year)1, or nearly twice the global gross national product (Costanza et al. 1997). Our reliance on ecosystem goods (e.g. food) and services (e.g. nutrient cycling) has prompted many countries to invest substantially in habitat conservation and monitoring, natural resource management, and environmental planning (e.g. more than US$155 billion between 2004 and 2008 in the US alone: USGPO 2009). Whilst most agree on the need for healthy ecosystems, the
2010 The Authors. Journal compilation 2010 British Ecological Society
1120 A. D. Irving et al. merits and drawbacks of numerous approaches to best achieve and ⁄ or maintain them require careful consideration (Wilson et al. 2007). Where habitats have been degraded or lost, management options have often adopted a compensatory approach by focussing on techniques of rehabilitation that ultimately aim to re-establish functional and self-sustaining habitat through human intervention (Marzluff & Ewing 2001; Elliott et al. 2007). Numerous approaches to rehabilitation have been studied across terrestrial and aquatic ecosystems, ranging from relatively simple transplants of individuals to understanding the importance of spatial arrangement and heterogeneity of habitats (Oertli et al. 2002). Notably, rehabilitation programmes show varied levels of success, including outright failure, which underscores the limitations to current techniques as well as the inherent challenges involved in re-creating complex ecosystems (Fonseca, Kenworthy & Thayer 1998). Nevertheless, repeated testing has taught us that limits to successful rehabilitation may be based upon a combination of biological realities (e.g. tolerance of species to transplantation), spatial considerations (e.g. variability of environmental stress amongst sites), and temporal restrictions (e.g. timing of reproductive activity) (Paling et al. 2003; Elliott et al. 2007). Such insights have led to a growing awareness that limitations may be alleviated by tailoring techniques to the biology of the system under study, particularly the life-history strategies and dispersal or colonization potentials of target species (e.g. Rehounkova & Prach 2010). Coastal habitats provide enormous resources on a global scale (e.g. fisheries) but have proven sensitive to anthropogenic disturbances such as overfishing, pollutants that reduce water quality, and species invasions (Hughes 1994; Meinesz 1999; Connell 2007). In particular, seagrass meadows are frequently affected because their requirement for sandy and well-illuminated environments, such as estuaries and protected embayments, often places them near centres of human habitation (Larkum & West 1990; Ralph et al. 2006). Since 1879, coastal eutrophication, increased sedimentation and turbidity, disease, and meadow fragmentation through dredging and boating activities, have caused the loss of over 51 000 km2 of seagrass, 29% of the world’s total seagrass habitat (Waycott et al. 2009). Such losses threaten the significant ecological services that seagrasses provide (Duarte 2002; Orth et al. 2006), including the trapping and stabilization of sediments to reduce turbidity and coastal erosion (Orth 1977), high rates of primary productivity with associated nutrient cycling and carbon sequestration (Mateo et al. 2006), and the provision of food and habitat for numerous fish and invertebrates (Heck et al. 1995), including many of commercial value (Connolly 1994). Rehabilitation is often considered a worthwhile option for degraded seagrass habitats because many seagrasses are notoriously slow-growing such that natural recovery, if it occurs (Kendrick et al. 2002), may take anywhere from tens to hundreds of years (e.g. Posidonia spp.: Kirkman & Kuo 1990; Gonza´lez-Correa et al. 2005). Transplantation is by far the most common method trialled around the world, followed by the planting of collected seeds and cultured seedlings (Fonseca,
Kenworthy & Thayer 1998; Calumpong & Fonseca 2001). The overall success of such techniques is questionable (e.g. van Keulen, Paling & Walker 2003; Bell et al. 2008), with metaanalysis of seagrass rehabilitation projects in the USA identifying success rates of 35–50% (Fonseca, Kenworthy & Thayer 1998). Limitations to success are often underpinned by the severity of the physical environment, such as wave exposure and associated sediment mobility causing erosion of transplants (van Keulen et al. 2003), as well as problems of seed supply and seedling culture (Holbrook, Reed & Bull 2002). There may be additional ethical issues to consider, such as the very real potential for transplantation to damage and fragment donor meadows, exacerbating the original problem by causing a local net loss of seagrass (Bull, Reed & Holbrook 2004). In essence, there is a clear need for fundamentally different approaches to seagrass rehabilitation in order to overcome current limitations, and a more careful consideration of lifehistory traits of target species may provide novel and achievable solutions. This paper presents an 8-year study that experimentally tests the performance of multiple seagrass rehabilitation methods that utilize fundamentally different ecological approaches. In the temperate waters adjacent to the coastal city of Adelaide in South Australia (population 1Æ2 million), at least 5200 ha of seagrass have been lost since the 1930s as a consequence of coastal eutrophication from wastewater inputs promoting the growth of epiphytes that smothered seagrasses and limited their capacity to photosynthesize (Neverauskas 1987; Shepherd et al. 1989). In recent years, the management of Adelaide’s wastewater has improved and a small amount of natural seagrass recovery has occurred in some areas (e.g. 4% near a major sewage outlet decommissioned in 1993: Bryars & Neverauskas 2004), suggesting successful rehabilitation may be possible. Therefore, we first tested the traditional and generic rehabilitation methods of (i) transplanting seagrass from healthy donor meadows into damaged sites, and (ii) seedling culture and outplanting, to asses their potential for large-scale rehabilitation. In general, the southern Australian coastline represents some of the most wave-exposed conditions in which seagrasses are found anywhere in the world (Walker & McComb 1992), and sediment instability following seagrass loss appears to be a critical factor limiting natural recovery by preventing the establishment of new recruits (Clarke & Kirkman 1989; Shepherd et al. 1989), as well as the retention of transplants (Paling et al. 2003). Consequently, traditional techniques may not always be practical, and so we developed and tested a novel approach that alleviates limits imposed by sediment mobility and which also exploits a critical seagrass life-history trait to maximize recruitment potential. This technique essentially involves deploying sand-filled bags of hessian (made from jute fibres, also known as burlap) on the sea floor to provide a stable sediment environment and to also facilitate the recruitment of seagrass seedlings possessing a distinctive ‘grappling hook’ at their base (see Materials and methods for further details). This novel technique was compared to the performance of the more generic and traditional rehabilitation methods to assess
2010 The Authors. Journal compilation 2010 British Ecological Society, Journal of Applied Ecology, 47, 1119–1127
Linking life-history to rehabilitation 1121 the benefits of a tailored approach that exploits a useful lifehistory trait and specifically alleviates a major limitation to successful rehabilitation.
Materials and methods
around the base of all plugs to stabilize surrounding sediments, with all transplants located within 1–2 m of remnant patches of seagrass. The survival of transplants was monitored for eight months, with the change in shoot density amongst surviving transplants calculated as an indicator of transplant expansion or contraction. Differences between techniques (plugs vs. sprigs) were tested using anova.
STUDY SITES
SEEDLING CULTURE AND OUTPLANTING
All research was done in the waters of Gulf St Vincent, South Australia, from 2003 to 2010. Gulf St Vincent is a large ( 6800 km2) and relatively shallow embayment (10 years to manifest due to naturally slow expansion rates of most seagrasses (Kirkman & Kuo 1990; Gonza´lez-Correa et al. 2005). Analyses proceeded by first comparing amongst-site variation in recruit densities over time for each experiment (rm-anova), and then comparing across experiments by analyzing the density and growth of recruits at 12 months (anova).
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Survival of transplanted seagrass after eight months varied from 0 to 80% depending on site, species, and technique. Plugs of both species survived relatively well at Henley Beach (75–80%), but survival at West Beach was lower, with fewer H. nigricaulis surviving relative to A. antarctica (15 vs. 55%; Fig. 1a). Survival of sprigs was also greater at Henley Beach (44–61%), with no sprigs surviving past June at West Beach due to erosion of the hessian matting (Fig. 1b). Across sites and species, 56% of transplanted plugs survived, compared to only 26% of sprigs. Average shoot density of surviving transplants declined over time in all treatments. For A. antarctica, the decline was relatively small for both plugs (mean ± SE = 17Æ25 ± 7Æ15%) and sprigs (13Æ08 ± 13Æ52%), and did not differ between techniques (anova: F1,24 = 0Æ23, P = 0Æ637). Greater declines were seen in H. nigricaulis where plugs lost almost twice as many shoots as sprigs, on average (35Æ05 ± 5Æ58% vs. 21Æ17 ± 17Æ15%, respectively), though such differences were not statistically significant (anova: F1,22 = 3Æ55, P = 0Æ073).
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Fig. 1. Survival of transplanted (a) plugs and (b) sprigs of A. antarctica and H. nigricaulis at Henley Beach and West Beach during 2003.
however, were not statistically significant (anova: F1,49 = 3Æ94, P = 0Æ053). Outplanted seedlings experienced substantial mortality, particularly on hessian bags placed within natural seagrass where no seedlings survived more than three months (Fig. 2b). Up to 10% of seedlings placed on sand survived for eight months, but low overall survival meant no differences between sites or habitats were formally detected (rm-anova: F1,6 = 2Æ46, P = 0Æ100). Considerable growth was observed amongst the few survivors (4Æ28 ± 0Æ78 cm, all on sand at Grange), which all appeared healthy after eight months.
SEEDLING CULTURE AND OUTPLANTING
RECRUITMENT FACILITATION
Survival of cultured P. angustifolia seedlings declined over time, falling to 6–9% after 11 months, and did not differ between beach- and meadow-collected fruits (Fig. 2a; rm-anova: F1,6 = 1Æ57, P = 0Æ256). Seedlings that did survive to 11 months generally appeared healthy, with beachcollected fruits exhibiting, on average, nearly twice as much growth as their meadow-collected counterparts (6Æ03 ± 1Æ12 cm vs. 3Æ67 ± 0Æ61 cm, respectively). Such differences,
Recruitment of A. antarctica seedlings to hessian bags occurred in all experiments, though it was spatially variable. In 2004, recruit densities at Grange were greater than at Semaphore over much of the first year, peaking at 345 ± 35 individuals m)2, but became similar between sites by 12 months (Fig. 3a, Table 1). In 2005, maximum densities of 238–349 individuals m)2 occurred at all but the two southern-most sites (Seacliff and Brighton), with densities declining to near zero for all sites
2010 The Authors. Journal compilation 2010 British Ecological Society, Journal of Applied Ecology, 47, 1119–1127
Linking life-history to rehabilitation 1123 (a) 100
a commonly observed pattern being a decline to lower but sustained densities over the life of the experiment (Fig. 3a–c). The magnitude of the decline was site dependent, with long-term densities reaching zero in some places but up to 72 individuals m)2 in others (best seen at Grange in Fig. 3a–c). Additionally, close observation of hessian bags at each sampling time showed that most had either become buried in the sandy sea floor and ⁄ or undergone severe or total degradation after 18–24 months in situ, such that their capacity to facilitate further recruitment was probably exhausted.
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Fig. 2. Mean (± SE) survival of P. angustifolia seedlings (a) grown in culturing tanks during 2004, and (b) outplanted into the field during 2005. Cultured seedlings were grown from fruits collected at local beaches and from meadows in situ, whilst outplanted seedlings were placed on sand or within natural seagrass at Grange and Semaphore.
except Grange over the following 12 months (Fig. 3b, Table 1). For bags deployed in 2007, recruitment was generally poor at all sites until after May 2008, when bags at Brighton and Grange supported a moderate number of recruits after 12 months ( 45 ± 11 individuals m)2 and 134 ± 23 individuals m)2, respectively), whilst those at Semaphore and Largs Bay supported few recruits (Fig. 3c, Table 1). Comparing recruit densities at 12 months across all experiments emphasized the spatial and temporal variation. Amongst years, 2005 produced the least recruits, whilst spatial variation was most obvious in 2007 (Fig. 4, anova comparison amongst sites: F10,98 = 14Æ85, P < 0Æ001). Interestingly, bags at Grange consistently retained the most recruits. For the experiment established in 2007, growth over the initial 12 months varied amongst sites from 0Æ50 ± 1Æ15 cm at Semaphore to 3Æ20 ± 1Æ07 cm at Brighton, though no differences amongst sites were detected (anova: F3,19 = 1Æ14, P = 0Æ360). Densities of A. antarctica were sampled for an additional 1–2 years beyond the first 12 months of each experiment, with
The cumulative loss of almost one-third of the world’s seagrass meadows over the past 130 years (Waycott et al. 2009) underscores the need to conserve and rehabilitate such that the valuable resources and ecosystem services that seagrasses provide are maintained (Duarte 2002; Orth et al. 2006). Seagrass rehabilitation has a reasonably long history (since Addy 1947) that emphasizes donor-dependent techniques, particularly transplants (see table 1Æ6 in Fonseca, Kenworthy & Thayer 1998). Whilst often suitable for small areas (£1 ha; Orth et al. 2006) in sheltered locales, transplant success is limited by numerous physical and biological features of the environment, as frequently demonstrated in the more exposed waters of southern Australia (Paling et al. 2003; van Keulen et al. 2003). Additionally, techniques such as transplants and seedling culture usually require a large commitment of time and resources that may render them impractical over large-scales. This paper shows how tailoring rehabilitation techniques to the biology of the target system or species may provide solutions that alleviate current critical limitations to rehabilitation success. The performance of traditional and generic transplant methods of rehabilitation was mixed off the coast of Adelaide. Plugs generally out-performed sprigs in terms of survival ( 56 vs. 26%, respectively), consistent with studies in Western Australia using a related species (A. griffithii: van Keulen et al. 2003) and also with species in other regions (e.g. Phyllospadix torreyi in California: Bull et al. 2004). In Western Australia, strong water motion during storms excavated sprigs of A. griffithii before they could fully establish. In our study, sprigs failed completely at West Beach, which exhibited greater wave energy that excavated and dislodged the hessian matting used to anchor sprigs. Fewer plugs also survived at West Beach, but survival did not reach zero, suggesting plugs are a better choice than sprigs in places of stronger wave energy and sediment movement (van Keulen et al. 2003). Importantly, shoot density declined in almost all transplants, suggesting constraints on other aspects of transplant establishment and growth. Tests of seedling culture and outplanting as a donor-independent method have been successful elsewhere (e.g. Italy: Balestri, Piazzi & Cinelli 1998), but proved challenging in our study. An earlier pilot study produced 95% survival of seedlings after six weeks (S. Seddon, unpublished data), in contrast to the poor survival (6–9%) after 11 months in the current
2010 The Authors. Journal compilation 2010 British Ecological Society, Journal of Applied Ecology, 47, 1119–1127
1124 A. D. Irving et al. (a) 400
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experiment. A combination of excessive epiphyte growth on leaves and the 90% shadecloth used to condition seedlings to light intensities at outplanting sites may have reduced survival by limiting light availability. In a previous study, Kirkman (1978) controlled epiphytes on adult Zostera capricorni by blocking all light for three days, but since seedlings are unlikely to have sufficient carbon stores in their rhizome to survive such periods of darkness, it was questionable whether such complete shading would have also severely impacted seedlings in our study.
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Fig. 3. Mean (± SE) density of A. antarctica recruits on hessian bags deployed in (a) 2004, (b) 2005, and (c) 2007. Broken lines indicate the samples taken after bags had been in situ for 12 months.
Outplanted P. angustifolia seedlings also performed poorly, with only 10 seedlings, 2% of those planted, surviving for eight months. Similar trials using P. australis in Western Australia, however, had greater success (30% survival after 11 months, J. Statton pers. comm.). Poor survival of outplanted seagrass seedlings is common (Holbrook et al. 2002; Bull et al. 2004, but see success in Balestri et al. 1998), yet juveniles of most species naturally experience high mortality (e.g. Holbrook et al. 2002). On balance, natural bottlenecks in juvenile survival may be difficult to overcome even
2010 The Authors. Journal compilation 2010 British Ecological Society, Journal of Applied Ecology, 47, 1119–1127
Linking life-history to rehabilitation 1125 Table 1. Results of repeated measures-anovas testing for spatiotemporal differences in the density of A. antarctica seedlings on hessian bags during the first 12 months from deployment in 2004, 2005, and 2007 Year
Source
2004
Site Error Time Time · Site Error
1 18 5 5 90
487630Æ43 7499Æ50 49383Æ51 20234Æ04 6126Æ75
65Æ02
