Enhanced Production of Finfish and Large Crustaceans by Bivalve Reefs
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Several bivalve families include species that occur in sufficient densities to modify the environment and create structured biogenic habitat. These habitats have also suffered among the highest losses of any marine habitat globally. In the case of bivalve reefs, the physical structure provided by the shells, supplied with biodeposits produced from filter feeding, supports a high density of macroinvertebrate prey, as well as providing shelter for many juvenile fish. This combination leads to enhanced fish production when compared to the unstructured sediment; the habitat type which typically replaces bivalve reefs when they are destroyed. Measuring the densities of juvenile fish and crustaceans on oyster reefs, and at unstructured control sites provides a measure of the net increase in juvenile fish and large crustaceans supported by oyster habitat. Applying growth and mortality schedules from fishery stock assessment literature allows an estimate of the increased lifetime production of juveniles by oyster reef habitats. Species may also benefit from oyster reefs at later life history stages, but these potential benefits have not been included in the current estimates of production. Services such as increased fish production have been used to highlight the range of stakeholders, in addition to the oyster fishers, that benefit from oyster habitat. The broader constituent base for bivalve habitats includes groups such as recreational anglers and commercial fishers as well as the industries that support them. Engaging with these stakeholders through quantifying the benefits of bivalve habitats to fisheries has proven an invaluable asset in promoting bivalve habitat restoration globally, as well as in drawing more funding into restoration efforts. Furthermore, quantifying fish production introduces the potential to include habitats such as those produced by bivalves in Ecosystem-based Fisheries Management.
KeywordsFish production Bivalve habitat Oyster reef Mussel bed Ecosystem services Ecosystem-based fisheries management
Abstract in Chinese
摘要:当某些双壳贝类家族的个体密度达到一定程度时,它们可以改变环境并形成结构化的生物栖息地。这类栖息地的消亡也属于全球性海洋栖息地损失的范畴。双壳贝礁,通过贝壳形成物理结构,以摄食活动产生的生物沉积物作为营养物质来源,为众多的大型无脊椎动物提供,并为许多幼鱼提供栖息场所。与非结构化底质相比,这种底质环境会促进鱼类产量提高; 而当这种贝壳礁被破坏时,栖息地的类型往往也会改变。通过对比测量牡蛎礁和对照地点的幼鱼和甲壳类动物的密度,可以衡量牡蛎礁型栖息地对于幼鱼和大型甲壳类动物净增长的促进作用。应用渔业资源评估文献中的生长和死亡率时间表,我们可以估算牡蛎礁类栖息地对延长幼鱼生命周期的作用。许多物种在生命周期的末期可能会从牡蛎礁中受益。除了收获牡蛎外,一些业主也从牡蛎礁栖息地周围的鱼类产量增加而获益。 除了养殖户以及养殖企业,垂钓爱好者也是从双壳贝礁生态多样性的受益者。通过量化双壳贝礁对养殖企业的积极作用,并与企业进行合作是推动全球双壳贝类栖息地恢复工作的重要渠道和方式。此外,将鱼类养殖业中的各种因素进行量化可以更好地阐述牡蛎礁在生态系统水平渔业管理应用中的潜力。
15.1 Bivalves As Ecosystem Engineers Supporting Fish Production
Ecosystem engineers are organisms that modulate the availability of resources to other species, by causing physical state changes in biotic or abiotic materials (Jones et al. 1994). In the case of bivalve reefs,1 they create and maintain habitat primarily through the deposition of generations of shell (Gutiérrez et al. 2003, Walles et al. 2015), supplemented by a constant supply of biodeposits from filter feeding (Kellogg et al. 2013). The structure created by a matrix of shell provides shelter for many species and the biodeposits, in the form of faeces and pseudofaeces, supply concentrated nutrients to the benthic deposit feeders. It is the combination of shelter and protection from predation, combined with the biodeposits fueling a greater abundance of prey, that has long been considered as driving force for enhanced fish production by bivalve habitat (Humphries et al. 2011, Kesler 2015).
A range of bivalves fall into the category of ecosystem engineers. The primary groups that generate habitat are the oysters (Ostreidae) along with many species of mussels (Mytilidae). Other groups form aggregations dense enough to be considered as biogenic structure, such as the pearl oysters (Pteriidae), leaf oysters (Isognomonidae), and fan clams or penn shells (Pinnidae) (Gillies et al. 2015). However, relatively few current examples of high density reefs or beds (where the structured habitat has little vertical elevation) exist for these groups. There is also a lack of information on the historic extent of habitat formed by these groups which makes it difficult to determine their historic importance in forming biogenic structure.
Oysters and mussels are recognized worldwide as generating dense beds or reefs that may develop to a depth of many meters (Büttger et al. 2008, Todorova et al. 2009). As such they are the estuarine and higher latitude analogs of coral reefs, often consisting of substantial calcium carbonate structures with an outer veneer of living bivalves (Stenzel 1971, Walles et al. 2015). Bivalve habitats also support a generally diverse and dense array of associated organisms (Harding and Mann 2001). Although there is strong anecdotal evidence that mussel habitat is important for fish production, there are currently no quantitative measures of this impact. Restoration of mussel bed habitat is currently being undertaken on an experimental scale in Port Phillip Bay Australia (Mytilus edulis), and in the Haruki Gulf of New Zealand (Perna canicularis), along with the penn shell (Atrina zelandica), with the aim of improving water quality and for the production of fish, in particular pink snapper (Pagrus auratus), a popular recreational species (www. http://reviveourgulf.org.nz/). Similarly, the fishing community of El Manglito near La Paz, Mexico have traditionally lived from fishing in the Ensenada and La Paz Bay. This community has linked the functional extinction of the pen shell habitat in the Ensenada de La Paz with the collapse of the finfish stocks in this once productive bay, and are planning the restoration of the pen shell habitat as a recovery strategy for the finfish fishery (B. Hancock, personal communication).
15.2 History of Quantifying Fish Production from Oyster Habitat
Oysters have long been fished by coastal communities (Rick and Erlandson 2009). Since the first century AD the Romans imported oysters from as far afield as southern England (Philpots 1890). The rise of mechanised fishing led to the global collapse of oyster stocks (Beck et al. 2011). Consequently, oyster restoration efforts have long been part of the wild oyster fishery in many parts of the world (Saville-Kent 1894; Ogburn et al. 2007). It is, however, only recently that work in the United States paved the way for oyster habitat restoration for the multiple services provided by this habitat, in addition to the oyster fishery (e.g. enhanced water quality and shoreline protection; Petersen et al. 2019; Ysebaert et al. 2019). This is a conservation action that has gained a high level of support as the ecosystem service benefits that oyster habitats provide have become better understood.
One compelling service is the increased production of finfish and large crustaceans. Much of the early thinking behind quantifying the fish production from oyster habitat came from Federal Government mandates in the United States. One initial driver of oyster habitat restoration was a government-legislated requirement to restore the public resources injured by discrete environmental incidents such as chemical or oil spills, the release of pollutants from an identifiable catastrophic event, or from physical damage to the habitat such as dredging for port expansion or land reclamation (e.g. NOAA 1977). The initial legislation was described in the Comprehensive Environmental Response, Cleanup and Liability Act (CERCLA 1980) and the Oil Pollution Act (OPA 1990). For each incident addressed under such legislation the damage first needed to be quantified, prior to designing restoration to make the community ‘whole’. These laws helped develop both the practice of oyster habitat restoration and the initial methods to measure fish production from oyster habitat as an additional service to be accounted for. The acts dictate that restoration is undertaken to compensate the public for losses or injuries to natural resources under public ownership and held in trust by government managers and that restoration includes the services that those natural resources would have provided. This legislation continues to influence the quantification of ecosystem services from multiple habitats, including bivalve habitat, and is being expanded in the US section of the Gulf of Mexico through the Restore Act (2012), legislating the response to the Deep Water Horizon oil spill (available at https://www.treasury.gov/services/restore-act/Pages/home.aspx).
A parallel driver of oyster habitat restoration stems from the conservation communities interest in restoring this previously abundant and ecologically significant habitat. While the increasing number of comprehensive studies documenting and quantifying the loss of oyster habitat are essential for setting a realistic order of magnitude for the amount of habitat that might be restored (Beck et al. 2011; zu Ermgassen et al. 2012, 2013; Alleway and Connell 2015; Gillies et al. 2015), simply understanding the loss does not, by itself, generate the incentive to fund and support restoration at the required scale. Given the expense and time required for successful restoration, it has become increasingly necessary to quantify the services provided by the restored oyster habitat in order to place a monetary value on those services and demonstrate the tangible gain society receives from their restoration. Quantifying the expected tonnage of fish and large crustaceans produced per unit area of restored oyster reef has been a powerful way to demonstrate the value of oyster habitat to society and the return on the investment in oyster habitat restoration (C. Gillies, TNC, personal communication).
An additional motivation to quantify the fish production from marine habitats was the concept of Essential Fish Habitat (EFH) which was introduced to fishery management in many jurisdictions from the mid 1980s (e.g. Minns et al. 2011) and in the US in 1996 through the Magnusson-Stephenson Fishery Conservation and Management Act. The Act linked fish production to habitat, attempting to expand the focus of fishery management to include consideration of the capacity of the ecosystem to produce fish, rather than focusing purely on limiting extraction from stocks of the target species (Pikitch et al. 2004). The legislation also had the effect of focusing attention on how to measure the impact of habitat on fish production (Peterson et al. 2000). The concept of certain habitats being limited but important to one or more life history stages and, therefore, the overall success of a fish population, is among the most fundamental questions in fisheries ecology, and the foundation of the concept of EFH. When applied to the early life history stages, generally referred to as juvenile fish habitat, it recognizes that the early life history stages are typically those with the highest mortality rates and where small changes in survival can have large impacts on the number of individuals surviving to older cohorts.
The changes in habitat dependence of different age classes of many fish and large crustaceans complicates the measurement of the relative values of fish production by habitat for these species. A complete accounting of fish production would require assessing the contribution of habitat to fish production by individual age classes of fish. One alternative is to focus on one year class, simplifying the investigation to a level that can be measured and applied (e.g. Levin and Stunz 2005). The 0+ year class is the most abundant and also usually subject to the highest rates of mortality. Consequently, nursery habitats that impact the survival of this cohort will have the greatest influence on the lifetime production.
15.3 Current Status of Quantifying Fish Production Enhancement by Oyster Habitat
Quantitative data on the degree to which fish and macroinvertebrates are enhanced by bivalve habitats are rare outside of the United States. While there has been recent progress in understanding the role of Modiolus modiolus in Europe as an important habitat for the commercially important whelk Buccinum undatum (Kent et al. 2016, 2017), for most bivalve habitats outside of the U.S. evidence is limited to historical documentation of species counts (e.g. Moebius 1883; Riesen and Reise 1982). In order to quantify the enhancement of fish and invertebrate production by bivalve habitats, it is necessary to measure the abundance of the target age classes within the habitat, relative to where that habitat is absent. As such, repeated and paired density data from the contrasting habitats are essential in supporting such quantification.
By collating available paired on and off oyster reef fish and invertebrate data from 31 studies in the United States, zu Ermgassen et al. (2016a) identified species for which the juveniles were consistently found at higher abundances on oyster habitats as opposed to unstructured mud and sand habitat. These habitats often replace oyster reefs when lost, and were therefore considered the most suitable control habitat for comparison. As in Peterson et al. (2003), the authors found that the presence of oyster reef enhanced species at both the juvenile and later life history stages. They also found marked differences between biogeographical regions with regards to the species of fish and invertebrates enhanced by oyster reefs, with 12 species in the Mid and South Atlantic and to 19 species in the Gulf of Mexico enhanced as juveniles, and two and five species respectively at later life history stages.
Species found by zu Ermgassen et al. (2016a) to derive growth enhancement from C. virginica oyster reef in the Gulf of Mexico and in the South and Mid-Atlantic (zu Ermgassen 2016a)
Proportion of individuals caught on oyster reefs (%)
Gulf of Mexico
Black Sea bass
15.4 Assumptions and Limitations of the Current Approach
The approach developed initially by Peterson et al. (2003) and further developed by zu Ermgassen et al. (2016a) has provided a novel opportunity to gauge the lifetime benefits of nursery habitats to fish and invertebrate populations. The benefits that can be attributed to nursery habitats from reduced juvenile mortality are substantial and otherwise extremely challenging to capture. The approach is, however, dependent on the application of established fish growth and mortality models used in fishery stock assessment and as such should be caveated by the same underlying assumptions. Estimates of fish and invertebrate growth were derived by applying the von Bertalanffy growth curve to juveniles. In order to do so, various life history traits need to be known. These traits (length at infinite age, the constant K, and the length at time equals zero) are themselves estimated and may therefore be subject to some error. Estimated natural mortality is also required for the model. Mortality is one of the greatest sources of uncertainty in fisheries models (Rosenberg and Restrepo 1994), especially at smaller size classes as mortality derived from the field is often reliant on fisheries size classes. In order to reduce, as far as possible, the uncertainty in the mortality estimates applied, zu Ermgassen et al. (2016a) used the size dependent mortality equation developed by Lorenzen (2000), so as to better represent the higher mortality suffered by the small size classes of fish and invertebrates represented in the model.
It is universally known that any model is only as good as the data it uses. While oyster reefs in the U.S. are the best studied in the world, zu Ermgassen et al. (2016a) point out that some of the differences in fish and invertebrate enhancement between regions are still likely due to a lack of data and differing sampling efforts or techniques between regions. As such, the inclusion of more data in the model can only serve to improve the resulting estimates of the benefits of oyster reefs as nursery habitats. The data handling approach used required that species were represented in at least two different estuaries in order for that species to be included in the assessment. It is therefore possible that some rarer species, or species which are not as effectively captured using density-specific capture techniques (e.g. drop traps, seines), are currently missing from the existing estimates. A larger number of studies seeking to quantify the enhancement of the fish and invertebrate community by oyster reefs can only serve to improve the current model.
One important assumption of the model that is highlighted in zu Ermgassen et al. (2016a) is that the bivalve habitat must be limiting in the site of interest. The model provides an estimate of the per unit area enhancement of the fish and invertebrate community by oyster reef habitats. The authors argue that in the current landscape of extreme loss of oyster and other bivalve habitats globally it is likely that, for species whose juveniles are enhanced by oyster reef presence, habitat is in fact limiting. As such the addition of habitat should result in a greater number of individuals surviving to larger size classes. The authors, however, concede that should substantial areas of oyster reef be restored, other factors may well start to limit the production and the assumed linear relationship between habitat area and juvenile enhancement would cease to exist. The point at which this would happen is likely to be highly species dependent and the position of any such threshold, or even how to derive it, remains unknown. As such, it is important to bear this assumption in mind when planning large scale restoration or recovery of oyster habitats, so as not to oversell the potential of oyster reef in supporting fisheries as an ecosystem service in these later stages of oyster habitat recovery.
A further consideration is the effect of habitat redundancy, or the interaction between structured habitats in close proximity, on the nursery function of oyster reefs. Oyster reefs close to alternative structured habitats, such as seagrasses and saltmarshes may not result in the same, or indeed any, observable enhancement of juvenile fish (Grabowski et al. 2005; Geraldi et al. 2009), most likely because the abundance of an equivalent structured habitat can provide similar food and shelter to oyster reefs. This is, however, certainly not always the case, with some studies finding that oyster reefs in seagrass and saltmarsh landscapes enhanced invertebrate (Grabowski et al. 2005) and fish (Stunz et al. 2010) communities. An assessment of the interaction between the different types of essential fish habitat, when they occur in close proximity, will be important for fine tuning the overall estimates of fish production from structured habitat on an estuary scale.
15.5 Making the Results Available
The calculator is designed to allow users to enter data such as existing oyster density and mean size, expected oyster density and mean size for the restored habitat, and adjust the target % of the estuary volume to be filtered by oysters within the residence time of the estuary (see also Smaal and van Duren 2019). Existing data such as estuary volume, the residence time of water within the estuary, mean summer water temperature, and the historic percentage of estuary filtration achieved by the biomass of oysters present at the earliest available census (generally around 1900), and even recent existing oyster size and density values, are provided where available. The site calculates the area of oyster habitat that would need to be restored to achieve the specified level of filtration and the number and weight of fish, by species, that would be produced from that area of restored oyster habitat. Making these results available in real time during planning conversations is intended to facilitate setting objectives for oyster habitat restoration based on the filtration and fish production services returned at a system scale.
The model results provided in the calculator represent the mean production across the whole of a region. It is therefore critical that local knowledge be used to adapt the results to more accurately reflect the estimated production at a given site of interest. There are likely to be local factors that affect the availability of one or more species within the suite of species identified as being enhanced by oyster habitat (Humphries and La Peyre 2015). The ability to account for these local variations in species abundance has therefore been built into the calculator. There are options to set the production for any species to zero if the species is deemed absent from the site or rare. There is the option to use the average production from the meta-analysis, or even the upper confidence interval if there is evidence that a species is particularly abundant in the estuary being considered.
15.6 Management Applications
The major threat responsible for the reduction of bivalve habitat globally has been overharvest. In fact, the estimated 85% reduction in oyster habitat over the last approximately 100 years (Beck et al. 2011) is itself an underestimate, as most of the historical surveys undertaken around the end of the 1800s or early 1900s, and used as a baseline measure of the historical extent of oyster habitat, were conducted because of concerns that overfishing had already depleted the oyster stocks (zu Ermgassen et al. 2012, 2016b). Much of the subsequent depletion of these habitats has occurred because managers of the fisheries have been responding to the inputs and concerns of only one stakeholder group interested in the habitat; the bivalve fishers. Managers, or the politicians they advise, have therefore been focused solely on the landings of bivalves rather than considering those landings as just one of a number of legitimate services to be considered when managing the bivalve resource. Recognizing that the recreational and commercial fishers, that benefit from the fish and crustaceans produced by the oyster habitat, are also stakeholders with a legitimate interest in the bivalve habitat, along with members of the associated fish processing and recreational support industries, has the potential to change the view of managers responsible for that resource. The same can be said for the constituents connected to the other services provided by bivalve habitats described in this book, such as water quality from filtration and denitrification or increased coastal resilience from shoreline protection (Brumbaugh et al. 2010; Ferreira and Bricker 2019). Similarly, managing oyster resources for harvest alone has tended to focus the emphasis on replenishment activities or put-and-take management intended to increase the supply of oysters for harvest or the amount of shell substrate available for the recruitment of juvenile oysters and their subsequent harvest. This does not consider that oyster biomass and the condition of the oyster reef may be important factors influencing the provision of additional services as well as the long-term sustainability of the restored reef (Grabowski et al. 2012). Demonstrating the value of the finfish and crustaceans produced from oyster habitat is a powerful tool for supporting the protection of at least a portion of the remaining bivalve habitat and investing in the restoration of additional habitat.
Having estimates of the fish production from oyster habitat well documented and available, if only for a small region given the global distribution of biogenic bivalve habitats, provides the ability to influence fisheries management in two important ways. It provides the logic for fundamentally changing the paradigm for managing the fishery, based on consideration of the multiple stakeholder groups impacted by changes in the level of services provided by bivalve habitats, in addition to harvest. It also introduces the option of including bivalve habitat in the management considerations for the finfish and large crustacean species supported by those habitats, in a truly Ecosystem Based Fishery Management (EBFM) scenario.
Ecosystem based fisheries management has been a goal for many fisheries managers for many years and has been adopted to various extents by most fisheries management agencies worldwide (e.g. Fletcher et al. 2010). Most management agencies also recognize that there is still a long way to go, in order to approach comprehensive EBFM (Berkes 2012). Developing habitat specific fish production measures for oyster habitat has generated interest in developing similar measures for multiple essential fish habitats. Analogous measures are currently available from seagrass in southern Australia (Blandon and zu Ermgassen 2014) and shrimp from seagrass in Queensland, Australia (Watson et al. 1993). The development of models to estimate the fish and large crustacean production are currently underway for salt marsh and seagrass habitats from the US and from mangrove habitat globally (Hancock and zu Ermgassen, personal communication). The US studies of fish production from salt marsh and seagrass habitats include provision for engaging the fisheries management community in considering how measures of fish production from habitat can be included in fisheries management decisions (NOAA, National Marine Fisheries Service, personal communication), a potentially productive direction for the development of EBFM.
A definition of ‘reef’, and ‘biogenic structure’ are given in Appendix 1 of the Natura2000 Marine documents at http://ec.europa.eu/environment/nature/natura2000/marine/docs/appendix_1_habitat.pdf.
Bivalve reefs are alternatively referred to as shellfish reefs in many publications.
The authors are grateful to Dr. B. Walles and an anonymous reviewer for their constructive comments on the manuscript.
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