Ensuring seed quality in ecological restoration: native seed cleaning and testing

Seeds are a critical and limited resource for restoring biodiversity and ecological function to degraded and fragmented ecosystems. Cleaning and quality testing are two key steps in the native seed supply chain. Optimizing the practices used in these steps can ensure seed quality. Post‐collection handling of seeds can have a profound impact on their viability, longevity in storage, and establishment potential. The first section of this article describes seed cleaning, outlines key considerations, and details traditional and novel approaches. Despite the growth of the native seed industry and the need for seed quality standards, existing equipment and standards largely target agricultural, horticultural, and commercial forestry species. Native plant species typically have complex seed traits, making it difficult to directly transfer existing cleaning and quality standards to these species. Furthermore, in ecological restoration projects, where diversity is valued over uniformity crop standards can be unsuitable. We provide an overview and recommendations for seed quality testing (sampling, purity, viability, germinability, vigor), identity reporting, and seed transfer as well as highlight the need to implement internationally recognized standards for certification for native seeds. Novel and improved cleaning and testing methods are needed for native species from a range of ecosystems to meet the challenges and goals of the United Nations Decade on Ecosystem Restoration. The guidelines outlined in this article along with others in the Special Issue of Restoration Ecology “Standards for Native Seeds in Ecological Restoration” can serve as a foundation for this critical work.     

Effects of storage,mucilage presence,photoperiod, thermoperiod and salinity on germination of Farsetia aegyptia Turra (Brassicaceae) seeds: implications for restoration and seed banks in Arabian Desert

Seed viability and germination are key factors in the success of restoration efforts, especially when stored seeds are used. However, the effect of seed storage on germination of most of the native Arabian species is not well documented. We investigated the effect of storage time and role of the seed mucilage in regulating germination, dormancy, salinity tolerance and consequential survival strategy of F. aegyptia in an unpredictable arid desert setting. Effect of light and temperature during germination was studied under two photoperiods and two thermoperiods using intact and de-mucilaged seeds. Presence of mucilage and thermoperiod did not affect the germination. However, seed collection year and photoperiod had a highly significant effect on the germination. Increasing salinity levels decreased the germination of F. aegyptia but ungerminated seeds were able to germinate when salinity stress was alleviated. Seed storage at room temperature enhances the germination percentage, indicating that F. aegyptia seeds have physiological dormancy and it can be alleviated by after-ripening at dry storage. In addition, F. aegyptia seeds show ability to germinate at lower salinity concentration and remain viable even at higher saline conditions, indicating their adaptability to cope with such harsh environmental conditions.     

Collection and production of native seeds for ecological restoration

The global push to achieve ecosystem restoration targets has resulted in an increased demand for native seeds that current production systems are not able to fulfill. In many countries, seeds used in ecological restoration are often sourced from natural populations. Though providing seed that is reflective of the genetic diversity of a species, wild harvesting often cannot meet the demands for large‐scale restoration and may also result in depletion of native seed resources through over harvesting. To improve seed production and decrease seed costs, seed production systems have been established in several countries to generate native seeds based on agricultural or horticultural production methods or by managing natural populations. However, there is a need to expand these production systems which have a primary focus on herbaceous species to also include slower maturing shrub and tree seed. Here we propose that to reduce the threat of overharvest on the viability of natural populations, seed collection from natural populations should be replaced or supplemented by seed production systems. This overview of seed production systems demonstrates how to maximize production and minimize unintended selection bias so that native seed batches maintain genetic diversity and adaptability to underpin the success of ecological restoration programs.     

Restoring the Victorian Western (Basalt) Plains grassland. 1. Laboratory trials of viability and germination, and the implications for direct seeding

Summary   The Victorian Western (Basalt) Plains grassland is one of Australia's most threatened plant communities. Practitioners using seed for its restoration need to know whether seed can be sown fresh or whether it requires an after-ripening period. This study assessed the viability and germination of freshly harvested wild seed from 64 grassland species indigenous to the Basalt Plains of western Victoria. The seed was collected as part of a broader experiment that examined the potential of direct-sown complex seed mixes for the restoration of grassland communities. The germination of fresh seed at 25°C varied widely between species. Comparisons with tetrazolium viability tests for each species indicated varying levels of dormancy within the species pool. Germination separated into three broad responses at day 28. One-third of the species failed to germinate, one-third germinated at 1% to 50% and the remaining species germinated between 51% and 100%. Therefore, if the aim of a sowing was the rapid and synchronous establishment of most of the sown species, the use of fresh seed in restoration could be problematic. After 3 months of dry storage, eight species were re-tested for germination. Each of the selected species had shown high viability but low initial germination. Only two species significantly increased their total germination at 25°C. The annual species, Triptilodiscus pygmaeus , increased its total germination from 6% as fresh seed to 99% after dry storage. Testing the viability and germination capacity of freshly harvested seed from a large and diverse sample of native grassland species demonstrated that many of the species were unlikely to germinate rapidly or synchronously when sown in complex seed mixes soon after harvest. This finding has implications for the scheduling and management of restoration projects that rely on the use of such seed.     

Innovative Techniques for Large‐scale Seagrass Restoration Using Zostera marina (eelgrass) Seeds

The use of Zostera marina (eelgrass) seeds for seagrass restoration is increasingly recognized as an alternative to transplanting shoots as losses of seagrass habitat generate interest in large‐scale restoration. We explored new techniques for efficient large‐scale restoration of Z. marina using seeds by addressing the factors limiting seed collection, processing, survival, and distribution. We tested an existing mechanical harvesting system for expanding the scale of seed collections, and developed and evaluated two new experimental systems. A seeding technique using buoys holding reproductive shoots at restoration sites to eliminate seed storage was tested along with new techniques for reducing seed‐processing labor. A series of experiments evaluated storage conditions that maintain viability of seeds during summer storage for fall planting. Finally, a new mechanical seed‐planting technique appropriate for large scales was developed and tested. Mechanical harvesting was an effective approach for collecting seeds, and impacts on donor beds were low. Deploying seed‐bearing shoots in buoys produced fewer seedlings and required more effort than isolating, storing, and hand‐broadcasting seeds in the fall. We show that viable seeds can be separated from grass wrack based on seed fall velocity and that seed survival during storage can be high (92–95% survival over 3 months). Mechanical seed‐planting did not enhance seedling establishment at our sites, but may be a useful tool for evaluating restoration sites. Our work demonstrates the potential for expanding the scale of seed‐based Z. marina restoration but the limiting factor remains the low rate of initial seedling establishment from broadcast seeds.     

Spicing up restoration: can chili peppers improve restoration seeding by reducing seed predation?

Seed predation by rodents presents a significant barrier to native plant recruitment and can impede restoration seeding efforts. In nature, some plants contain secondary defense compounds that deter seed predators. If these natural defense compounds can be applied to unprotected seeds to inhibit rodent granivores, this approach could improve restoration seeding. Capsaicin is the active ingredient in chili pepper (Capsicum spp.) seeds that creates the burning sensation associated with human consumption of hot peppers. This compound has a similar effect on other mammals and is believed to have evolved as a deterrent to rodent seed predators. We used seed‐coating techniques to attach powder ground from Bhut Jolokia (Capsicum chinense) peppers to native plant seeds and evaluated the efficacy of these seed coatings for deterring rodent seed predation and enhancing native plant recruitment using laboratory and field experiments. Laboratory feeding trials demonstrated that native deer mice (Peromyscus maniculatus) consumed far fewer pepper‐coated seeds compared to untreated control seeds. Field seed‐addition experiments consistently demonstrated that rodent seed predation reduced native plant recruitment over the 4‐year study. Coating techniques used in the first 3 years were not persistent enough to reduce rodent seed predation effects on plant recruitment. However, a more persistent coating applied in conjunction with late‐winter sowing negated rodent seed predation effects on recruitment in year 4. Our results demonstrate that coating seeds with natural plant defense compounds may provide an effective, economical way to improve the efficacy of plant restoration by deterring seed predation by ubiquitous rodent granivores.     

黄土丘陵沟壑区主要物种植冠种子库动态及其生态策略

植冠种子库是植物适应环境并应对外界干扰的种子生态策略之一,研究了黄土丘陵沟壑区12种主要植物植冠种子库动态,结果表明:杠柳不具有植冠种子库,其他11种植物均具有植冠种子库;除了黄刺玫种子在翌年5月达到脱落高峰,其他植物大部分种子在冬季脱落,其中杠柳、达乌里胡枝子、茭蒿、黄柏刺和水栒子的大部分种子脱落集中偏早,铁杆蒿和土庄绣线菊的大部分种子脱落集中偏晚;植冠宿存对大部分植物种子的萌发特性表现为促进作用;但不同植物种子的萌发时滞对植冠宿存响应差异较大;9种植物种子在植冠上宿存至翌年2月底,其种子活力仍能维持达60%以上;该区植物表现出不同的植冠种子库策略,通过不同的方式来减少干扰的威胁,提高成功萌发与更新的几率,它们或具有较大规模的宿存量、或调控种子萌发特性、或提高种子维持活力的百分比。此外,全面了解该区植物形成植冠种子库的机理及对应的生态策略还有待于全面、深入的研究。     

Ten years of native seed certification in Germany – a summary

Many renaturation projects and compensation areas are based on the use of seeds from regional indigenous wild plants; in the following: native or regional seeds. Despite this, such seeds make up only a small proportion of the total number of seeds used for greening projects; in Germany, for example, it is only around 1% (=200 t per year). Although the market for regional seeds is small, it is highly competitive. High‐priced native seeds compete with flower mixes of unspecified origin and can only be differentiated from them by reliable quality seals. A quality assurance system based on seed legislation (EU Directive 2010/60, preservation mixtures) has been developed in a few European countries. However, quality assurance ends with the sale of the seeds. Thus, seed use remains unmonitored, and often unsuitable material, or material foreign to the region, is planted in restoration areas. Unfortunately, nature conservation has not made seed‐based restoration one of its key issues, neither at the European nor at the national level. Currently there are many different local and regional standards, methods and private certificates that are confusing for users and which provide little continuity and predictability for producers. We recommend the establishment of an EU directive or a broadly agreed recommendation to the EU member states, spearheaded by nature conservation, which would define the standards for producing and using native seeds (e.g. harmonised regions that cross national borders, quality regulations). At the same time, wild plant interest groups should combine existing structures in order to strengthen seed‐based restoration through international cooperation.     

Protocols for Use of Potamogeton perfoliatus and Ruppia maritima Seeds in Large‐Scale Restoration

Restoration of submerged aquatic vegetation from seed has been hampered by a lack of information on the appropriate conditions for collecting, processing, and storing seeds prior to dispersal. Seeds must be processed and stored under conditions that maintain seed viability, meet dormancy requirements, and prevent premature germination. This study examined the effects of collection date, processing technique, aeration, storage and induction temperature and salinity, and storage period on seed germination of two mesohaline aquatic species, Potamogeton perfoliatus and Ruppia maritima. Collection date and processing technique were significant factors affecting seed yield from donor populations. Seeds of both species remained viable and germinated best when stored at 4°C, and then exposed to freshwater induction conditions. However, their responses to other factors differed. Aeration during storage was necessary in order to maintain viability of P. perfoliatus seeds, whereas it was unnecessary for R. maritima seeds. Storage in freshwater at 4°C prevented germination of P. perfoliatus seeds, while high salinity during cold storage was necessary to minimize premature germination of R. maritima. Mean germination time of P. perfoliatus was dependent on storage salinity; in contrast, mean germination time of R. maritima seeds was dependent on induction salinity. These differences indicate that the methods required to produce large quantities of underwater plant seed amenable to large‐scale restoration efforts must be tailored to the specific requirements of individual species and must consider the range of processes from initial harvest through seed testing prior to field establishment.     

International principles and standards for native seeds in ecological restoration

The growing demand for native seeds in ecological restoration and rehabilitation, whether for mining, forest, or ecosystem restoration, has resulted in a major global industry in the sourcing, supply, and sale of native seeds. However, there are no international guidance documents for ensuring that native seeds have the same standards of quality assurance that are regular practice in the crop and horticultural industries. Using the International Principles and Standards for the Practice of Ecological Restoration as a foundation document, we provide for the first time a synthesis of general practices in the native seed supply chain to derive the Principles and Standards for Native Seeds in Ecological Restoration (“Standards”). These practices and the underpinning science provide the basis for developing quality measures and guidance statements that are adaptable at the local, biome, or national scale. Importantly, these Standards define what is considered native seed in ecological restoration and highlight the differences between native seeds versus seeds of improved genetics. Seed testing approaches are provided within a logical framework that outline the many different dormancy states in native seed that can confound restoration outcomes. A “pro‐forma” template for a production label is included as a practical tool that can be customized for local needs and to standardize reporting to end‐users on the level of seed quality and germinability to be expected in a native seed batch. These Standards are not intended to be mandatory; however, the guidance statements provide the foundation upon which regulatory approaches can be developed by constituencies and jurisdictions.     

Message in a bottle: Inadvertent loss of seeds of native grassland species as a result of rudimentary long‐term storage

Many practitioners are likely to have collected seeds with the intention of using that seed for conservation and/or restoration plantings, but have not got around to using the seed, sometimes for many years. Currently, it is not clear what species have short‐lived or long‐lived seed when stored under rudimentary conditions such as in paper bags or in a refrigerator. We report the germinability of 12 temperate native grassland species, comprising 16 populations, whose seeds were collected with the purpose of raising seedlings to plant into the wild, but whose seeds were subsequently stored at ~2–4°C for 25+ years. We conclude that most of the grassland species that we assessed do not have viable seed after 25 years when stored in such conditions; only two species germinated despite evidence that seed germinates well for most species when first collected. Inadvertent loss of seeds of as a result of long‐term storage is most likely in readily germinable species (e.g. members of the Asteraceae). The ways in which seeds are stored by practitioners deserves consideration given the risk of seed mortality with long‐term storage under rudimentary conditions.     

Native Seed Collection, Processing, and Storage for Revegetation Projects in the Western United States

The foundation of a successful revegetation or restoration program is quality native seed. This requires careful collection, processing, and storage. Mature seed should be collected from healthy, local stands with a sufficiently broad genetic base. Careful identification of the site characteristics and seed-lot tracking are essential. Yearly variation in seed production and seed quality can be very high, and an early determination of seed quality can prevent expensive failures. Nondestructive evaluation using X-rays is effective and economical, but techniques such as staining, inspection, and germination tests can also be helpful. Cleaning, dewinging, and upgrading seed before storage can (1) reduce weight and bulk, (2) improve storage life, (3) increase germination, and (4) make greenhouse production and field planting easier and more economical. The seeds of many native plants can lose their viability quickly if they are not stored under controlled conditions. Seeds in storage must also be protected from rodents, pests, and disease. Dormancy is common in the seeds of many native species, and experimentation is often necessary to determine the best way to break seed dormancy. This can be complicated by year-to-year and plant-to-plant variation.     

Dormancy and germination: making every seed count in restoration

From 50 to 90% of wild plant species worldwide produce seeds that are dormant upon maturity, with specific dormancy traits driven by species' occurrence geography, growth form, and genetic factors. While dormancy is a beneficial adaptation for intact natural systems, it can limit plant recruitment in restoration scenarios because seeds may take several seasons to lose dormancy and consequently show low or erratic germination. During this time, seed predation, weed competition, soil erosion, and seed viability loss can lead to plant re‐establishment failure. Understanding and considering seed dormancy and germination traits in restoration planning are thus critical to ensuring effective seed management and seed use efficiency. There are five known dormancy classes (physiological, physical, combinational, morphological, and morphophysiological), each requiring specific cues to alleviate dormancy and enable germination. The dormancy status of a seed can be determined through a series of simple steps that account for initial seed quality and assess germination across a range of environmental conditions. In this article, we outline the steps of the dormancy classification process and the various corresponding methodologies for ex situ dormancy alleviation. We also highlight the importance of record‐keeping and reporting of seed accession information (e.g. geographic coordinates of the seed collection location, cleaning and quality information, storage conditions, and dormancy testing data) to ensure that these factors are adequately considered in restoration planning.     

Effects of Moisture, Temperature, and Time on Seed Germination of Five Wetland Carices: Implications for Restoration

Successful restoration of sedge meadow wetlands is limited by lack of information regarding reintroduction of sedge (Carex) propagules. While restoration from seed is common for prairie restorations, little is known about the germination characteristics of many wetland plants, including sedges. We present the results of a 2.5-year study on seed germination and viability for five species of Carex common to sedge meadow and prairie pothole wetlands in temperate North America. Seed storage and germination conditions were investigated to determine the optimum combination for maintaining seed viability and stimulating germination rates over time. Seeds were germinated under seven different temperature and three moisture regimes after storage for 4, 10, and 14 months under one of four different storage regimes (dry-warm, dry-cold, moist-cold, and wet-cold). The efficacy of short-term wet-cold stratification to stimulate germination of 2.5-year-old seed after long-term dry storage was also investigated. Carex stricta, Carex comosa, and Carex lacustris showed the greatest germination response after wet-cold or moist-cold storage, while Carex lasiocarpa and Carex rostrata showed similar rates of germination after either wet-cold or dry-warm storage. Wet-cold long-term storage was associated with a high level of viability in all five species after 2.5 years. Viability and germination rates were reduced in Carex stricta, Carex comosa, and Carex lasiocarpa after long-term dry-cold storage. Germination rates of seeds stored dry for 2.5 years are not improved by short-term wet-cold treatment in any species tested. Carex seeds should be stored under wet-cold conditions to maintain seed viability over time, thus increasing the likelihood of seeding success for sedge meadow restoration.     

Testing Broadcast Seeding Methods to Restore Urban Forests in the Presence of Seed Predators

Forest restoration in urban areas often occurs in isolation from remnant forest, limiting the chances for recolonization by native species. Plants with bird‐dispersed seeds can be particularly vulnerable to dispersal limitation and regeneration can be further impeded by non‐native seed predators. We used a factorial experiment to investigate broadcast seeding as a method to reintroduce trees with large seeds and fleshy fruits into early successional forests. We assessed rates of seed and fruit loss, germination and seedling establishment in three seed treatments: (1) caging to exclude introduced mammalian seed predators; (2) removal of fleshy fruit pericarp; and (3) placing seeds in nutritionally enriched clay balls. Across all species (Beilschmiedia tawa, Elaeocarpus dentatus, and Litsea calicaris) seeds and fruits accessible to mammalian predators suffered significantly greater loss (58%) than those protected by cages (4%). However, seed and fruit loss in the presence of predators was reduced to only 35% across all species by the treatment combining the removal of fruit flesh and clay ball application to seeds. Establishment of B. tawa seedlings after 1 year was significantly enhanced by the clay ball treatment (12% of seeds sown vs. 6% without clay balls). Very low establishment rates were recorded for E. dentatus and L. calicaris. Broadcast seeding was found to be a viable method of improving regeneration of large‐seeded late successional trees and may be a cost‐effective alternative to planting saplings. Seedling establishment can be improved with fruit flesh removal and clay ball treatments, especially in the presence of mammalian seed predators.     

In situ or ex situ seed conservation: which is the more effective way to maintain seed longevity of an endangered cactus?

With restricted populations and a small number of individuals, Discocactus bahiensis Britton & Rose (Cactaceae) is an endangered species in Brazil and its capacity for the formation of seed banks in the soil and the maintenance of seed viability remains unknown. Thus, the aim of the present study was to determine the most efficient way to maintain viability during storage of seeds of D. bahiensis . Seeds were stored in paper bags and either kept in a cold chamber (7 ± 2°C) in the dark (ex situ conservation) or buried in the soil to a depth of 5 cm in an area of natural occurrence of the species (in situ conservation). Germinability of the seed banks was evaluated monthly for 20 months. During the first 10 months of storage, germinability of the seeds conserved in situ and ex situ was similar to that of recently collected seeds. After this period, a 70% reduction in germinability was found for the seeds maintained in situ and there was nearly complete loss of viability after 12 months of storage in the field (germinability < 10% in the last 8 months of the experiment), indicating the ability to form persistent soil seed banks. In contrast, the seeds stored in the cold chamber maintained greater than 70% germinability throughout the entire analysis period, demonstrating that ex situ conservation is the most efficient way to maintain the viability of the seeds of this endangered species.     

Insects remove more seeds than mammals in first‐year prairie restorations

Seed sowing is a common early step in restoration, but seed consumers can impede plant establishment and alter community structure. Moreover, seed consumers vary in feeding behaviors and the relative importance of different seed consumer groups during restoration are not well understood. At 12 first‐year prairie restorations in Michigan, we studied seed predation using seed removal trays to ask: What is the relative magnitude of seed removal by insects and mammals? Do seed removal rates change over the growing season? Do habitat edges influence seed removal? At what rates are 10 prairie plant species' seeds removed by mammals and insects? Seed removal depended on consumer type, time of year, and seed species. Insects accounted for the majority of seed removal, contrary to previous research in similar systems. In May, insects removed 1.8 times more seeds than mammals, while in August, they removed 5.1 times more. There was greater seed removal in August. During May 28% of seeds were removed, compared to 54% of seeds removed during August, an increase driven by insects. Edge proximity did not influence seed removal. Certain seed species were removed more than others. For example, Lespedeza capitata (round‐headed bush clover) was always removed at high rates, whereas Coreopsis lanceolata (lance‐leaved coreopsis) and Andropogon gerardii (big bluestem) were always removed at low rates. Mammals and insects showed different preferences for several species. This research suggests a prominent role of seed predation, particularly by insects, for early prairie restoration dynamics, with influences varying temporally and among species.     

黄土区露天煤矿排土场不同微地貌土壤种子库特征

黄土区露天煤矿排土场边坡水力冲刷强烈，不同植被恢复模式与水力作用耦合形成的不同微地貌可通过对种子的不同拦截作用而影响植被的恢复及发展。为了探讨排土场不同微地貌对种子的拦截效益及不同植被恢复模式的恢复潜力，选取不同恢复模式下形成的细沟、丛岛和草带三种微地貌为研究对象，以邻近裸坡为对照，研究不同微地貌土壤种子库特征及其拦截力。结果表明：（1）在不同微地貌中土壤种子库均以一年生藜科和禾本科植物为主；丛岛微生境的土壤种子库中有较丰富的物种和较高的多样性指数。（2）各微地貌的土壤种子库均具有表层聚集现象；草带微地貌中的土壤种子库总储量最大，且草带的0-2 cm土层处的土壤种子库密度显著高于各微地貌的各个土层（P<0.05）。（3）细沟和丛岛在上坡位对种子的拦截效果更好，草带在下坡位对种子的拦截效果更好。综上所述，沙蒿恢复模式形成的丛岛有利于增加土壤种子库的物种多样性，草带有利于增加土壤种子库的储量，故在黄土区排土场进行植被恢复时可以利用不同微地貌对土壤种子库分布特征的优势构建适宜的复合植被恢复模式。     

Seed germination requirements of Trembleya laniflora (Melastomataceae), an endemic species from neotropical montane rocky savannas

Trembleya laniflora is an endemic shrub from neotropical montane rocky savannas of southeastern Brazil. It has been indicated as a potential candidate for ecological restoration of abandoned iron‐ore mines due to heavy metal accumulation. Here, we evaluated the seed germination requirements of T. laniflora. Seeds collected in 2005 and 2008 were set to germinate under a broad range of temperature and light conditions. Seed viability was estimated by dissecting seeds under a dissecting microscope for embryo presence/absence. Seeds were photoblastic and optimum temperature range was 20–25°C, coinciding with the onset of the rainy season. Seeds were viable after 42 months of storage, which together with small seeds that easily get buried and light requirement for germination suggest formation of soil seed banks. Except the large fraction of embryoless seeds, almost all tested seeds germinated when incubated under light conditions; therefore, T. laniflora should be regarded to have nondormant seeds. Easiness of burial resulting from small seed size and positive photoblastism may both contribute to incorporation into soil seed banks. Our data suggest that the long‐term storage of T. laniflora seeds provides a useful strategy for plant reintroduction.     

Role of Brycinus lateralis (Teleostei: Alestidae) in dispersal and germination of Nymphaea nouchali (Angiospermae: Nymphaeaceae) seeds on a seasonal floodplain of the Okavango Delta,Botswana

Seed passage through the gut of vertebrates can be important for seed dispersal, but might influence seed viability. The ability of seeds to germinate after ingestion by seed-eating fish is important for the population dynamics of some plant species, and significant in the evolution of plant–fish interactions. Certain fish in the Okavango Delta, Botswana, are fruit- and seed-eaters and could act as seed dispersers. We sampled 14 fish species in 2013, finding Nymphaea nouchali var. caerulea seeds in the digestive tracts of eight, most commonly in the striped robber Brycinus lateralis. Seeds extracted from the gut of this species had an overall mean germination success of 11.7%. This fish species might well be a legitimate seed disperser, having a positive effect on seed dispersal from parent plants in the Okavango Delta. The current study represents one of the first investigations of the likelihood of seed dispersal by fish on the African continent.