SEAWEED IN THE TROPICAL SEASCAPE Stina Tano
Seaweed in the tropical seascape Importance, problems and potential
Stina Tano ©Stina Tano, Stockholm University 2016 Cover photo: Eucheuma denticulatum and Ulva sp. All photos in the thesis by the author. ISBN 978-91-7649-396-0
Printed in Sweden by Holmbergs, Malmö 2016 Distributor: Department of Ecology, Environment and Plant Science To Johan
I may not have gone where I intended to go, but I think I have ended up where I intended to be.
Douglas Adams
ABSTRACT The increasing demand for seaweed extracts has led to the introduction of non-native seaweeds for farming purposes in many tropical regions. Such intentional introductions can lead to spread of non-native seaweeds from farming areas, which can become established in and alter the dynamics of the recipient ecosystems. While tropical seaweeds are of great interest for aquaculture, and have received much attention as pests in the coral reef literature, little is known about the problems and potential of natural populations, or the role of natural seaweed beds in the tropical seascape.
This thesis aims to investigate the spread of non-native genetic strains of the tropical macroalga Eucheuma denticulatum, which have been intentionally introduced for seaweed farming purposes in East Africa, and to evaluate the state of the genetically distinct but morphologically similar native populations. Additionally it aims to investigate the ecological role of seaweed beds in terms of the habitat utilization by fish and mobile invertebrate epifauna. The thesis also aims to evaluate the potential of native populations of eucheumoid seaweeds in regard to seaweed farming.
The initial results showed that non-native E. denticulatum is the dominating form of wild eucheumoid, not only in areas in close proximity to seaweed farms, but also in areas where farming has never occurred, while native eucheumoids are now scarce (Paper I). The low frequency of native E. denticulatum in seaweed beds, coupled with a low occurrence of reproductive structures, indicates that the effective population size may be low, which in turn may be a threat under changing environmental conditions. These results, combined with indications that seaweeds may be declining in East Africa, illustrates the need for attaining a better understanding of the ecological role of tropical seaweed habitats. The studies on the faunal communities of seaweed beds showed that they are species rich habitats, with high abundances of juvenile fish and mobile epifauna (Paper II and III), strongly indicating that these habitats should be considered for future seascape studies and management actions. Productivity in East African seaweed farming is decreasing, and as the current cultivation is based on a single non-indigenous haplotype, a more diverse genetic base has been suggested as a means to achieve a more productive and sustainable seaweed farming. Although our results show that East African E. denticulatum has a lower growth rate than the currently used cultivar (Paper IV), the several native haplotypes that are present in wild populations illustrates that, though a demanding endeavour, there is potential for strain selection within native populations.
LIST OF PAPERS This thesis is based on the following papers, referred to in the text by their Roman numerals (I-IV):
I Tano SA, Halling C, Lind E, Buriyo A, Wikström SA (2015). Extensive spread of farmed seaweeds causes a shift from native to non-native haplotypes in natural seaweed beds. Marine Biology, 162, 1983–1992. doi:10.1007/s00227-015-2724-7 II Tano SA, Eggertsen M, Wikström SA, Berkström C, Buriyo AS, Halling C. Tropical seaweed beds as important habitats for juvenile fish in an East African seascape. (submitted) III Tano SA, Eggertsen M, Wikström SA, Berkström C, Buriyo AS, Halling C. Tropical seaweed beds are important habitats for mobile invertebrate epifauna. (submitted) IV Halling C, Tano SA, Eggertsen M, Buriyo AS, Msuya FE, Wikström SA. The introduction of South East Asian seaweed and its ecological implications; Can native East African Eucheuma denticulatum and Kappaphycus alvarezii be a potential alternative for farming? (manuscript)
My contributions: Planning and designing the study (Paper I-IV), collecting the data (Paper I-IV), performing genetic/laboratory analyses (Paper III- IV), analysing data (Paper I-IV) and writing the papers (main writer in Paper I, II and III, active participation in Paper IV).
Paper I is reprinted with kind permission from the publisher.
Contents
ABSTRACT ...... vii LIST OF PAPERS ...... ix OBJECTIVES OF THESIS ...... 12 INTRODUCTION AND SPECIFIC AIMS ...... 12 Seaweeds as resources ...... 12 Mariculture of eucheumoid seaweeds ...... 13 Eucheumoid seaweed introductions and spread outside farms ...... 13 Seaweed farming in East Africa ...... 17 Tropical seaweeds as habitats ...... 18 Productivity problems in seaweed farming ...... 23 METHODOLOGY ...... 24 Study area ...... 24 Study species ...... 26 Field surveys ...... 28 Biomass and epifauna samples ...... 28 Reproductive potential ...... 28 Seaweed farming ...... 28 Genetics ...... 29 KEY RESULTS AND DISCUSSION ...... 30 Spread of non-indigenous strains ...... 30 Seaweed beds as diverse habitats ...... 31 Potential to utilize native strains in seaweed farming ...... 32 SYNTHESIS ...... 32 FUTURE RESEARCH ...... 34 POPULÄRVETENSKAPLIG SAMMANFATTNING ...... 37 ACKNOWLEDGEMENTS ...... 39 Financial support ...... 40 LITERATURE CITED ...... 40 Abbreviations
EA East African SEA South East Asian WIO Western Indian Ocean OBJECTIVES OF THESIS This thesis investigates i) the spread of non-indigenous strains of the tropical macroalga Eucheuma denticulatum, introduced for seaweed farming purposes, as well as ii) the state of native populations of the eucheumoid species E. denticulatum and Kappaphycus alvarezii in East Africa. Additionally it aims to iii) elucidate the ecological role of tropical macroalgal beds, in terms of habitat utilization by fish and epifauna, and iv) evaluate the farming potential of native eucheumoid seaweeds.
INTRODUCTION AND SPECIFIC AIMS
Seaweeds as resources The term macroalgae is commonly used as an overarching description of a polyphyletic group of multicellular plant like organisms from the taxa Rhodophyta, Chlorophyta and Phaeophyceae. They do not possess true roots or a specialized vascular system, but anchors themselves to the substrate using holdfasts, hapters or rhizoids and nutrients are absorbed directly from the water column. Marine macroalgae, or seaweeds, exist throughout the coastal oceans of the world, and although the communities they reside in differ, they are a common feature of most coastal zones. Many macroalgal species have long been utilized by humans as food, feed, fertilizer and for medicinal purposes (Jones 1958; Zaneveld 1959), with many of the human uses originating in East Asia (Zaneveld 1959). Seaweeds are considered to have potential for bioremediation of waters polluted by fish farming (e.g. Troell et al 1997; Chopin et al 2001; Lüning and Pang 2003; Neori et al 2004; Huo et al 2012), and also as candidates for future CO2 reduction (e.g. Chung et al 2011; Sahoo et al 2012; Chung et al 2013). Currently they provide the human population with food, cattle feed and secondary metabolites used in food applications, biofuel, medicinal products and fertilizers (see e.g. Smit 2004; Zubia et al 2007; Matanjun et al 2009; Bixler and Porse 2011). Due to the many applications of seaweeds and a continuously increasing demand, what was once started as an unsustainable harvest of wild seaweeds (Parker 1974; Mshigeni 1984; Norambuena 1996), has now expanded into large scale seaweed cultivation. Seaweed farming currently produces over 25 million tonnes of algae annually at a global scale, with the production having more than doubled since the turn of the century (FAO 2014). Although a substantial part of the seaweed produced is still intended for direct human consumption, the continuously increasing demand
12 for secondary metabolites, such as carrageenan, has resulted in carrageenan containing seaweeds now being the most cultivated (FAO 2014). Carrageenans are sulphated polysaccharides found in the cell wall of certain red algae that exist in three main isomers (kappa-, iota- and lambda carrageenan) with different properties and uses. The main ones produced are kappa and iota, which are extracted from Kappaphycus alvarezii and Eucheuma denticulatum respectively (Bixler and Porse 2011), with kappa carrageenan being in greater demand globally and K. alvarezii therefore fetching a higher market price than E. denticulatum (Valderrama et al 2013).
Mariculture of eucheumoid seaweeds Carrageenan, initially procured by harvesting the temperate seaweed Irish moss (Chondrus crispus) (Stanley 1987), is now mainly obtained by the cultivation of the tropical eucheumoid species Eucheuma denticulatum and Kappaphycus alvarezii (FAO 2014). Both species occur naturally in South East Asia and East Africa, and were harvested for decades in both areas before unregulated collection resulted in population decline and decreased export (Mshigeni 1973; Parker 1974; Sen 1991). As a result, cultivation of eucheumoids started in South East Asia in the 1970’s (Parker 1974). Due to the success of eucheumoid farming, the South East Asian seaweeds and the farming technique were transferred to various locations of the tropical and subtropical world, both inside and outside the species native range. The main factors involved in enabling this rapid escalation of eucheumoid farming were the low level of technology and investments needed, as well as it being a potential alternative livelihood in rural areas (Pickering 2006). To date eucheumoid seaweeds have been introduced to more than 30 countries across the globe (Fig. 1) (Ask et al 2003a; Pickering 2006; Mallea et al 2014; Sellers et al 2015), but success of the cultivation has varied and they are currently only commercially farmed in a few countries (Valderrama et al 2015). However, eucheumoid production in these countries attains more than eight million tonnes wet weight annually (FAO 2014).
Eucheumoid seaweed introductions and spread outside farms The introduction and spread of non-indigenous seaweeds may lead to unpredictable and undesirable effects on native ecosystems, with the most common impacts being a reduction in abundance of native macrophytes and an altered community composition of the recipient ecosystem (Schaffelke and Hewitt 2007; Williams and Smith 2007). In seaweed aquaculture the selection of strains with suitable qualities is the key to high yields, and selection is commonly based on desirable traits, such as a high growth rate and vegetative propagation, as well as a high resistance against herbivory, epiphytes, diseases and abiotic stressors (Neish et al. 1977; Levy and
13 Friedlander 1990; Mollion and Braud 1993; Krann and Guiry 2000; Buschmann et al. 2001; Ask and Azanza 2002; Titlyanov and Titlyanova 2010). Some of the traits, such as high growth rates and vegetative reproduction, are suggested to be overrepresented among non-indigenous species that become very abundant and have a large impact on the recipient system (Andreakis and Schaffelke 2012). This indicates that there might be specific risks connected with the introduction of cultivated seaweeds to new geographical areas, as these have commonly undergone strain selection. However, when non-indigenous seaweeds are introduced for farming purposes, the ecological risks are weighed against the potential socioeconomic gain (Pickering et al 2007), and generally environmental aspects have not been taken into account at the time of introduction (Zemke- White and Smith 2006). The two main reasons for the introduction of eucheumoid seaweeds to new areas are the high demand for carrageenan and the socioeconomic potential for generating alternative livelihoods (Pickering et al 2007). Eucheumoid farming, being extractive rather than polluting, is commonly marketed as an environmentally benign alternative livelihood, and it has even been claimed that it might be environmentally detrimental to avoid an introduction, as the local community might then have to turn to destructive fishing methods (Ask 2003; Ask et al 2003a). Additionally, it has been claimed that once a cultivation is commercially operational, the risk of non-native seaweeds spreading to the wild will be negligible, as all loose lying seaweed fronds would be collected due to the economic incentive (Ask et al 2003a). These claims so far remain unsupported, and while it has been indicated that increased seaweed farming in combination with decreasing fish stocks, have led to a decrease in the number of fishers in some areas, this was not true for all localities investigated (Sievanen et al 2005; Hill et al 2012). Furthermore, it is not known whether there are any effects on the use of destructive fishing methods (Sievanen et al 2005). Regarding eucheumoid farming as environmentally benign, it has been shown that even though seaweed farming may be less detrimental than other aquaculture activities (e.g. Bryceson 2002; Pickering et al 2007), it can still have direct and indirect impacts on the flora and fauna in the farming areas (Johnstone and Olafsson 1995; Eklöf et al 2005; Eklöf et al 2006a; Eklöf et al 2006b).
Propagation of eucheumoid seaweeds may occur either by sexual reproduction and the spread of asexual spores, or by vegetative fronds breaking off in the seaweed farms and being transported to suitable habitat by tides and currents. Eucheumoid seaweeds commonly have a low frequency of sexual reproduction (e.g. Doty and Santos 1978; Lluisma and Ragan 1995) and low viability of spores (Bulboa et al 2008), and it is thought that the eucheumoids main mean of dispersal is vegetative (Doty 1987; Pickering et al 2007; Castelar et al 2009). However, even though sexual reproduction appears to be absent in some areas where they have been
14 introduced (Smith et al 2002; Castelar et al 2009), viable spores have been found on fronds being cultivated in the field in other locations (Bulboa and de Paula 2005). Initially it was believed that introduced eucheumoid seaweeds could not become established, as vegetative fragments were not able to form new holdfasts, or to spread over deeper waters as they are negatively buoyant (Russell 1983). However, since the late 1990’s it has been shown that introduced eucheumoids have become established outside of farms in a number of areas. Eucheumoid seaweeds have become nuisances in Hawaii, India and Panama (Conklin and Smith 2005; Chandrasekaran et al 2008; Sellers et al 2015), where they have been shown to overgrow and smother corals, and spread has so far been confirmed also in Fiji, Venezuela, Brazil and Tanzania (Ask et al 2003b; Barrios et al 2007; Ferreira et al 2009; Halling et al 2013). However, in most cases of introductions no scientific studies regarding the potential spread of eucheumoids from farming areas have been made (Zemke-White and Smith 2006).
Japan China Cuba Colombia Vietnam Micronesia Hawaii Cambodia Marshall Isl. Fr. Antilles India Mexico Venezuela Djibouti Kiribati Panama Guam Solomon Isl. Brazil Maldives Malaysia Tuvalu Kenya Indonesia French Polynesia Tanzania Mozambique Fiji Madagascar Philippines Vanuatu Tonga Samoa Introduction Confirmed spread Start of farming Cook Isl.
Figure 1. Map of eucheumoid introductions worldwide, as well as those countries were spread has been confirmed.
15 Figure 2. The off-bottom seaweed farming technique that is commonly used in Zanzibar.
16 Seaweed farming in East Africa The East African region differs from other locations of eucheumoid introductions as it harbours native, but genetically distinct, haplotypes of both Eucheuma denticulatum and Kappaphycus alvarezii (Zuccarello et al 2006). Large amounts of these native seaweeds were harvested for export from natural seaweed beds in the decades before the South East Asian (SEA) seaweeds were introduced (Sen 1991), but due to overharvest the populations in the natural seaweed beds declined in the early 1980’s (Mshigeni 1973; Pettersson-Löfquist 1995; Mshigeni, 1998). In 1989 SEA E. denticulatum and K. alvarezii were introduced to Zanzibar, Tanzania, for farming purposes (Lirasan and Twide 1993). As seaweed farming started, trials with native strains showed comparatively poor results, and native seaweeds were considered unsuitable for farming (Lirasan and Twide 1993; Pettersson-Löfquist 1995). The farming of SEA strains of E. denticulatum on the other hand, was highly successful and it soon became the dominant seaweed species farmed, whereas the more valuable K. alvarezii experienced problems with diseases and die-offs, resulting in it being farmed to a lower degree (Msuya 2011a). The high productivity of SEA strains lead to a rapid development of seaweed farming in many locations around Unguja and Pemba Islands (Pettersson-Löfquist 1995), and Zanzibar now has around 15 000 - 20 000 seaweed farmers (Msuya 2011b). In later stages the farming practices and SEA strains have been transferred to other locations in Tanzania, as well as other East African countries, such as Kenya, Madagascar and Mozambique (Yarish and Wamukoya 1990; Mollion and Braud 1993; Msuya et al 2014).
The most commonly used farming method in East Africa is the off-bottom technique, where ropes with seaweed fronds are stretched between stakes anchored in the substrate, usually in sandy areas or seagrass beds (Fig. 2). As in all commercial cultivation of eucheumoids, the propagation of plants is solely done by vegetative cuttings (Hurtado et al 2015), with the seeding material being taken from the last harvest. The farms are commonly placed in intertidal or shallow subtidal areas, and free-floating fronds that have broken off cultivation lines may be found drifting outside of farms (Halling et al 2013). In recent years non-indigenous SEA haplotypes of E. denticulatum has been found growing outside of farms (Halling et al 2013), indicating that an establishment of the introduced seaweeds may have occurred. When non-indigenous haplotypes of a native species are introduced there is a risk of a cryptic invasion, as they may easily be mistaken for their native counterpart. Such invasions have previously been described between morphologically similar species of algal taxa such as Polysiphonia, Ulva and Gracilaria, as well as for subspecies of Codium fragile (McIvor et al 2001; Solgaard Thomsen et al 2006; Baamonde López
17 et al 2007; Provan et al 2007). One example of a cryptic invasion within the species level in an aquatic environment is an introduced genotype of the common reed (Phragmites australis), that has replaced its native counterparts in many regions of North America (Saltonstall 2002). The introduced genotype has also spread into new environments (Chambers et al 1999; Vasquez et al 2005), and has been found to outcompete other species and alter community structure (Benoit and Askins 1999; Able and Hagan 2000). In the case of eucheumoid introductions to East Africa, they were mainly motivated by the high growth rate of the SEA seaweeds (Lirasan and Twide 1993), which in turn could be a competitive advantage in case of establishment. This raised the question of the extent of the spread of non- indigenous haplotypes, as well caused concern for potential impacts on native populations.
Paper I investigates the presence and extent of spread of non-indigenous haplotypes of Eucheuma denticulatum in four sites around Zanzibar, as well as the presence and extent of native haplotypes in natural settings. It also explores which haplotypes that are currently used in seaweed farms, as well as the spread of non-indigenous haplotypes within farming areas.
Research questions Paper I: Extensive spread of farmed seaweeds causes a shift from native to non-native haplotypes in natural seaweed beds
1. Which haplotypes of E. denticulatum are currently being used in farms? 2. Can non-indigenous haplotypes of E. denticulatum be found attached in close vicinity of active seaweed farms? 3. To what extent are native and non-indigenous haplotypes of E. denticulatum present in areas with naturally occurring eucheumoids? 4. Is hybridization between native and introduced haplotypes likely to occur?
Tropical seaweeds as habitats Tropical waters have long been recognized to commonly harbour a high species diversity of macroalgae and areas of rich macroalgal growth (e.g. Isaac 1960; Taylor 1968; Lawson 1969; Tsuda 1977). However, early accounts on tropical macroalgae have mainly focused on systematics (see
18 e.g. Gepp and Gepp 1908; Isaac 1967), and though they reveal the high diversity of macroalgae in the tropics, and occasionally comment on seaweed habitats being “rich” (Lawson 1969), “extensive” (Isaac and Isaac 1968) and “dense” (Taylor 1968), the description of relevant ecological data is often sparse. As seaweed as resources became of interest in larger parts of the tropical world, the focus also came to include the occurrence of commercial species, as well as the biomass of standing crop. Large amounts of seaweeds were harvested from certain tropical regions (Mshigeni 1973; Parker 1974), and studies indicated that both non-commercial and commercial seaweeds could be found in high abundances in tropical areas (e.g. Varma and Rao 1962; Isaac and Isaac 1968; Rao 1973; Wanders 1976; Chuang 1977; Mshigeni 1984; Untawale and Jagtap 1989; Yarish and Wamukoya 1990). Macroalgal distribution and abundance is affected by a number of factors, such as grazing, competition, physical tolerance and availability of light and nutrients (Lobban and Harrison 1997). In the tropics grazing pressure from both herbivorous fish and invertebrates, such as sea urchins, can be substantial, and herbivory has commonly been shown to restrict macroalgal distribution to shallower and more exposed areas (Randall 1961; Hay et al 1983), but exceptions to this generalization occur (Dahl 1973). The upward distribution may instead be restricted based on the tolerance to air exposure and the high temperature that commonly occurs in shallow tropical areas, due to high insolation and large tidal amplitudes (Tsai et al 2004; Cox and Smith 2011). The tolerance of tropical seaweeds to high temperatures is high, with growth optima as high as 25-30° C (Wiencke and Bischof 2012), but seasonality may occur with standing crops of macroalgae declining during the warm or cold season, depending on region (Trono and Lluisma 1990; Tsai et al 2004; Ateweberhan et al 2005; Fulton et al 2014).
In recent literature the majority of studies concerning tropical seaweeds (that do not involve systematics) appear to focus either on their uses to humans (see e.g. Zubia et al 2007; Matanjun et al 2009), or on the phase-shifts that can occur on stressed and overfished coral reefs, as coral mortality, increased nutrients and an absence of herbivorous fish may result in a dramatic increase in macroalgal abundance (McManus and Polsenberg 2004; Hughes et al 2007). This leads to an conspicuous dichotomy in the literature: on the one hand seaweeds are depicted as “saviours” which may provide future generations with food, feed and chemicals while reducing nutrient effluents from other types of aquaculture (e.g. Løvstad Holdt and Kraan 2011; Huo et al 2012; Radulovich et al 2015), while on the other hand they are depicted as the villains which are threatening the diversity and plenty of the coral reefs (e.g. Rasher and Hay 2010; Diaz-Pulido et al 2011; Jessen and Wild 2013). Few studies have, however, focused on the ecology of naturally occurring tropical seaweed beds (but see: Wilson et al 2010; Chaves et al 2013; Evans et al 2014). One potential reason may be that tropical seaweed beds have not
19 truly been considered as habitats, but have rather been considered and described as inhabitants of coral reef habitats, such as reef flats (see e.g. Morrissey 1980; McCook 1997; Costa et al 2000; Fox and Bellwood 2007; Wismer et al 2009) and back-reefs (McClanahan et al 1999), although macroalgae in some of these habitats may form assemblages that dominate in cover as well as community structure (Morrissey 1980; Trono and Lluisma 1990; Tanner 1995; Costa et al 2000; Fox and Bellwood 2007; Wilson et al 2010). Also the seasonality of macroalgae that has been shown to occur in some tropical regions, where the cover, height and assemblage structure may differ between seasons (Trono and Lluisma 1990; Vuki and Price 1994; Ateweberhan et al 2005), may further explain why seaweed assemblages have rarely been recognised as habitats, as they may be more variable than other habitats in tropical regions.
In temperate areas, seaweed assemblages provide complex habitats and feeding grounds to diverse assemblages of organisms (e.g. Duffy 1990; Christie et al 2003; Fredriksen et al 2005; Stål et al 2007), and additionally constitute important carbon sources for higher trophic levels, both in the areas where they grow and as allochthonous detrital material (Lenanton et al 1982; Duggins et al 1989; Dunton 2001; Wernberg et al 2006). They have been shown to harbour high diversity and abundances of epifauna (Christie et al 2009; Gestoso et al 2010), which may feed on the available algal resources (Duffy 1990; Viejo 1999), and constitute an important link between primary producers and higher trophic levels (Norderhaug et al 2005; Stål et al 2007). Temperate seaweeds also provide juvenile fish with refuge as well as feeding grounds, and have been shown to influence recruitment of several fish species positively (Jones 1984; Carr 1994; Levin and Hay 1996; Schmidt et al 2011). In tropical areas these functions have primarily been described for other macrophyte habitats, such as seagrasses and mangroves, which have been shown to positively influence fish recruitment of coral reef fish and commercial fish species (Lugendo et al 2005; Lugendo et al 2006; Olds et al 2012a; Berkström et al 2012), and may have high abundance and diversity of associated invertebrate fauna (Kwak and Klumpp 2004; Eklöf et al 2006a). However, also areas dominated by tropical seaweed assemblages have been found to harbour diverse invertebrate communities (Taylor 1968; Chuang 1977), and the few studies that have investigated the use of macroalgal beds by juvenile fish in other tropical regions have shown that they can indeed act as nurseries to a number of coral reef species (Wilson et al 2010; Chaves et al 2013; Evans et al 2014).
20
Figure 3. A shallow seaweed bed in Menai Bay, Unguja Island.
21 In East Africa the ecology of macroalgal beds is not well known, despite rich and diverse seaweed beds being present in the region (Fig. 3) (Mshigeni 1984; Yarish and Wamukoya 1990). There are, however, indications that the macroalgal assemblages in Tanzania have decreased in abundance and distribution over the last decades (Buriyo, pers. comm.). Once common species appear to have become scarce and a shift has occurred from native to non-native haplotypes of a common species (Tano et al 2015; Paper I). This indicates the importance of investigating the potential functions that these diverse habitats provide to associated fauna, as well as their overall ecological contribution as a part of the tropical seascape.
Paper II investigates fish assemblages of seaweed beds in Menai Bay, Unguja Island, Zanzibar, and looks into the potential utilization of seaweed beds as juvenile grounds. This is accomplished by comparing the seaweed fish communities to those of closely situated seagrass beds, which are known to be utilized as nurseries for a wide variety of fish species of commercial importance, as well as high importance for coral reef fish recruitment. Additionally, the paper investigates the size specific distribution of Scaridae, a fish family commonly found in both seaweed and seagrass beds.
Research questions Paper II: Tropical seaweed beds as important habitats for juvenile fish in an East African seascape
1. Do tropical seaweed beds act as juvenile grounds for coral reef fish and fish of local commercial importance? 2. Is there a size-specific distribution of Scaridae between seaweed and seagrass beds?
Paper III investigates the mobile epifaunal communities of tropical seaweed beds in Menai Bay, Unguja Island, Zanzibar, and evaluates their potential role as feeding habitats for invertivorous fish. This is accomplished by comparing the epifaunal assemblage of seaweed beds to that of closely situated seagrass meadows, which are macrophyte habitats previously shown to harbour taxon rich epifaunal communities and act as feeding grounds to a number of fish species. Additionally, it examines the role of macrophyte variables on the abundance and taxon richness of the epifaunal communities of seaweed and seagrass habitats respectively.
22
Research questions III: Tropical seaweed beds are important habitats for mobile invertebrate epifauna
1. What epifaunal communities are associated with seaweed beds and seagrass meadows respectively, and how do they differ between the two habitat types? 2. Can tropical seaweed beds act as feeding grounds for invertivorous fish? 3. Which macrophyte variables influence the abundance and taxon richness of the epifaunal communities of seaweed and seagrass beds respectively?
Productivity problems in seaweed farming Apart from the apparent risk of large scale spread of non-indigenous seaweeds from farms, the seaweed farming of eucheumoids has lately been facing increasing productivity problems. In South East Asia, as well as several of the countries where these seaweeds have been introduced, problems with epiphytes, diseases and pests are resulting in decreased production (Vairappan et al 2008; Hayashi et al 2010; Hurtado et al 2015). Ice-ice, a malady mainly attributed to poor water conditions where parts of the algal tissue becomes bleached and necrotic, can be a major contributor to fragmentation and loss of farmed algal fronds (Largo et al 1995). Moreover, epiphyte infestations such as Neosiphonia spp. may lead to bacterial infections and large scale die-offs (Vairappan et al 2008; Pang et al 2015), and herbivory by fish and sea urchins may remove substantial quantities of seaweeds (Russell 1983; Pang et al 2015). One of the suggested reasons for the productivity problems is that the majority of all currently farmed eucheumoids are based on a limited gene pool, as a result of the vegetative propagation within cultivation which has been ongoing since the start, in combination with the strain selection that has taken place (Hurtado et al 2015). As a consequence, there are now initiatives in the Philippines to explore a larger range of eucheumoid morphotypes from natural resources, in an effort to expand the genetic material of the seaweeds used for vegetative cultivation (Hurtado et al 2015).
Also in Tanzania productivity problems within the farms have increased, with epiphyte infestations, ice-ice and die-offs resulting in the abandonment of farming in some areas (Msuya 2011a; Msuya and Porter 2014). The
23 farming in Tanzania is based solely on seaweeds from South East Asia, and therefore struggles with the same restricted genetic resources, which may limit the potential for adaptation to environmental changes (Halling et al 2013). As one of the reasons for the die-offs of eucheumoids in Tanzania is thought to be the increased maximum seawater temperatures that have been observed since the 1990’s (Msuya 2011a), there is a great need to explore the potential for increasing the genetic variation of the cultivars used in seaweed farming.
Paper IV compares the growth rates, as well as susceptibility to epiphytes and herbivory, of native East African Eucheuma denticulatum and Kappaphycus alvarezii to that of the South East Asian E. denticulatum, to explore the farming potential of native seaweeds.
Research questions Paper IV: The introduction of South East Asian seaweed and its ecological implications; Can native East African Eucheuma denticulatum and Kappaphycus alvarezii be a potential alternative for farming?
1. How do native E. denticulatum and K. alvarezii perform in a seaweed farm setting, compared to SEA E. denticulatum? 2. Can native eucheumoids be potential alternatives for seaweed farming in East Africa?
METHODOLOGY
Study area Zanzibar is a semi-autonomous part of Tanzania, consisting of two main islands, Pemba and Unguja, with a population of approximately 1.3 million in 2012 and a population growth of around 2.8% yearly (NBS 2014). It is located in the Western Indian Ocean (WIO) and has a land area of around 2500 km2. The climate in the region is tropical and subject to monsoonal seasonality, with the South East monsoon occurring from March to October having cooler temperatures and lower solar insolation than the North East monsoon, which takes place from November to February (McClanahan 1988). The seascape around the islands contains a diverse array of different habitats such as coral reefs, seagrass meadows, mangrove forests and seaweed beds (see e.g. Berkström et al 2013a), and shallow areas are
24 subjected to large tidal amplitudes of around 4 meters at spring tide (Tobisson et al 1998).
The majority of the studies in this thesis have been performed in Menai Bay (Fig. 4); a 470 km2 multi-use conservation area in the south-west of Zanzibar, which encompasses six islands and a diverse tropical seascape of coral reefs, seagrass beds, mangroves and seaweed beds (Tobey and Torell 2006; Tyler et al 2011; Berkström et al 2013a; Berkström et al 2013b). Also covered in this thesis are various sites on the east coast of Unguja Island, which generally contains sand flats of varying width inside protective barrier reefs (Johnstone et al 1998), and commonly harbour seagrass meadows (e.g. Lyimo et al 2008; Alonso Aller et al 2014), smaller patch reefs and scattered areas of rocky substrate. One site on the east coast that differs from the other sites is Chwaka Bay, which contains a varied seascape of large seagrass meadows, mangroves and coral reefs as well as mud and sand flats (de la Torre-Castro and Lyimo 2012). In addition to this some sites in Pemba Island have also been included (to a lesser degree).
Kenya Tumbe Ras Kiuyu
Fundo Island
Zanzibar Pemba Islands Island
l e n n a Tanzania h C n r a a e ib c z O n a n Matemwe ia Z d In Unguja Sume Island Uroa Chwaka Bay Bweleo Paje Muungoni Fumba Jambiani Menai Bay Shungi Komonda
Mozambique 1 km
Figure 4. Map of Unguja and Pemba Islands, with all study sites of this thesis included. Close up shows study sites within Menai Bay.
25 Study species The focal species in Paper I is Eucheuma denticulatum, and to some extent Kappaphycus alvarezii and E. platycladum, whereas in Paper IV E. denticulatum and K. alvarezii are in focus (Fig. 5). All three species belong to the family Solieriaceae, of the tribe Eucheumatoideae, and are collectively referred to as eucheumoids (Wakibia et al 2006). All species of this tribe contains carrageenan, a secondary metabolite, imbedded in the cell wall. Eucheumoids are extremely morphologically plastic, which historically has led to systematic issues (Zuccarello et al 2006), and can come in a variety of colours and shapes. As this thesis deals with both native East African and introduced South East Asian E. denticulatum, it is important to note that there is currently no way of differentiating between native and introduced haplotypes in the field, but this must be done by genetic analyses.
Paper II and III studies seaweed beds dominated by species rich seaweed assemblages, containing such taxa as Sargassum, Turbinaria, Ulva, Eucheuma, Padina and Amphiroa, as well as seagrass meadows dominated by Thalassodendron ciliatum.
26
Figure 5. The many faces of Eucheuma denticulatum (A-F), where (B) is seaweed from a farm and the others are wild growing E. denticulatum. Photo (G) shows a typical form of wild growing Kappaphycus alvarezii and (H-I) E. platycladum.
27 Field surveys Belt transects (2x25 m) were used for the estimation of algal cover in Paper I, as well as for the visual census of fish in Paper II. In Paper I estimation of algal cover was made at four sites (Fumba, Komonda, Sume and Matemwe; Fig. 4), with estimation of coverage being made in 2 meter sections at the time, on a 9 graded scale (1, 5, 10, 15, 25, 50, 75 or 100% cover), and averages were calculated for each transect. In Paper II the estimation of fish abundance was made using temporally stratified belt transects (according to Samoilys and Carlos 2000), and mobile fish were counted at a first swim over the transect line, while the less mobile and cryptic fish were counted at a second swim. For Paper II the habitat variables were documented along the transect line by placing a square (0.25m2) every 5 meter of the transect line (n=5), with an average being calculated for each transect.
Biomass and epifauna samples In Paper I biomass samples of Eucheuma denticulatum were collected in squares (0.04m2) in areas where it was present at the investigated sites, and the wet weight was recorded. In Paper III squares (0.04m2) were placed haphazardly, in both seaweed beds and seagrass meadows, and all above ground macrophytes and fauna within the squares were collected in an attached bag. Samples were placed on ice and taken to the lab, where the epifauna was removed from the macrophytes and stored in 70% ethanol until sorting. The macrophytes were identified to lowest possible taxonomical level and dried to constant weight, after which dry weight was obtained. All fauna ≥1 mm were identified to lowest taxonomical level and counted, after which they were sorted into phyla and dried to constant weight, and weighed.
Reproductive potential In Paper I the presence of reproductive structures on Eucheuma denticulatum were investigated by visual examination of cross and longitudinal sections of fronds, using a light microscope, during three occasions of the high growth season of the seaweeds.
Seaweed farming In Paper IV Eucheuma denticulatum and Kappaphycus alvarezii, collected from a natural seaweed bed in Menai Bay, as well as E. denticulatum collected from a seaweed farm, were cultivated at three sites on the East Coast of Unguja Island. The cultivation followed the commonly used
28 farming practice in Zanzibar, where the seaweed fronds are tied to ropes, which in turn are attached to stakes driven into the sandy substrate. Before placement in the field, all fronds were weighed and genetic samples were taken in order to establish the origin and haplotype of each frond in the cultivation. After seven weeks of cultivation (approximately one farming cycle), the fronds were collected and brought back to the lab, where they were weighed, and the amount of epiphyte cover and herbivory were estimated.
Genetics Many seaweed species are morphologically plastic organisms, which entails that their shape and colour may vary extensively between different environmental settings. Eucheumoid species appear to be plastic to such an extent that even differentiating between species may sometimes be difficult (Zuccarello et al 2006), and the visual appearance of seaweed fronds are of little help in separating non-indigenous and native strains. To be able to definitively separate South East Asian from East African strains genetic methods have been necessary. We have utilized a conserved region of mitochondrial DNA (cox2,3) to separate native and non-indigenous haplotypes (Paper I&IV) of Eucheuma denticulatum, as well as to investigate the number of native and non-indigenous haplotypes present around Zanzibar of E. denticulatum, Kappaphycus alvarezii and E. platycladum.
For Paper I the seaweed fronds were picked haphazardly, over the entire areas of the different sites, to enable a credible assessment of approximate haplotype frequencies in natural seaweed beds. In addition, seaweed fronds were collected from cultivations around Unguja and Pemba Islands, and areas around farms were searched for attached E. denticulatum, which were sampled when found. In Paper IV larger quantities of both E. denticulatum and K. alvarezii were collected, and genetic samples were taken from all fronds that were used in the cultivation.
All samples for genetic analyses were dried and stored in silica gel, until later DNA extraction at Södertörn University (Sweden). It is however difficult to obtain high quality DNA from eucheumoid seaweeds, as the secondary metabolite they are farmed for, carrageenan, is difficult to remove from the samples and interferes in the DNA-extraction. Two different methods have been used during the course of the thesis work: i) a modified CTAB extraction described by Zuccarello and Lokhorst (2005), and ii) the E.Z.N.A.® Mollusc DNA kit, which is intended to purify DNA from tissues rich in mucopolysaccharides. The cox2,3 spacer was generated following Zuccarello et al. (1999), and PCR purification and Sanger sequencing were
29 performed by Macrogen Europe Inc. using an ABI3730XL sequencer. Following this the sequences were quality controlled and aligned using Mega 5.2. The mitochondrial DNA haplotypes were aligned and identified by comparison with sequences from Zuccarello et al (2006) and Halling et al (2013), and all sequences from Paper I are deposited in GenBank® (KT390538-KT390698).
KEY RESULTS AND DISCUSSION
Spread of non-indigenous strains Paper I shows that the introduced South East Asian haplotypes of Eucheuma denticulatum are dominating in natural seaweed beds, and that native haplotypes are now sparse. The study also shows that attached non- indigenous haplotypes can be found in a number of locations around Zanzibar, both in areas with seaweed farming activities, and areas where seaweed farming has never occurred. The presence of two different introduced haplotypes in natural seaweed beds, whereof only one has been cultivated during the last 10 years, illustrates that this spread is not dependent on a constant influx of new seaweed from the seaweed farms, but rather that the introduced seaweeds have established self-sustaining populations. This indicates that even if farming of introduced strains would be stopped, the SEA strains are likely to be present for the foreseeable future. The dominance of introduced SEA haplotypes at all the investigated sites, also where no seaweed farming has taken place, indicates that E. denticulatum has the potential to spread also longer distances. The study also shows that the main mode of reproduction for E. denticulatum in the region appears to be vegetative, as only two fronds with reproductive structures were found during the time of the study, which took place during the season of high growth. No fronds of the SEA strains were found to possess reproductive structures, and therefore it seems unlikely that the strains will hybridize. The results of the study, that the native haplotypes are now scarce and have a low frequency of sexual reproduction, indicates that the effective population size of native E. denticulatum could be very low. This illustrates a vulnerability of the species to changing climate conditions, as a small effective population may have a reduced fitness owing to factors such as inbreeding (Willi et al 2006). In addition, the study also found that other species of eucheumoids, which were once common, such as K. alvarezii and E. platycladum, are now very sparse and appear to have disappeared from areas where they were once found.
30 Seaweed beds as diverse habitats Paper II shows that seaweed beds in Zanzibar have high abundances of juvenile fish, particularly of juvenile coral reef fish and fish species of local commercial importance. The study also demonstrates that the abundance of these exceed that of seagrass beds, a known nursery habitat in the region (Lugendo et al 2005; Berkström et al 2012). Interestingly, it also appears that fish of the family Scaridae may preferentially utilize seaweed beds at smaller sizes (≤5 cm), while being found in seagrass beds predominantly at sizes above 5 cm. This indicates that fish species may utilize more than one vegetated habitat during their juvenile phase, and that seaweed beds may act as initial juvenile habitat. Such dependence by juveniles on multiple habitats, with seaweed habitats as initial juvenile habitat, has previously been shown for black-spot tuskfish in Southern Japan and red-eye parrotfish in Brazil (Yamada et al 2012; Feitosa and Ferreira 2015), indicating that this sort of preferential utilization of seaweed habitats may be occurring in several tropical regions. Multivariate analyses indicated that seaweed beds and seagrass meadows have differing fish assemblages despite both being vegetated habitats in relatively close proximity. Fish communities of seaweed beds were generally more homogenous in comparison to seagrass meadows, which is likely caused by the patchy distribution of larger multi- species fish schools in seagrass meadows. We found that fish species richness was higher in seaweed than seagrass habitat, and that juveniles from the families Muraenidae and Serranidae were only found in seaweed beds. On the other hand juveniles from the family Siganidae, which is commonly associated with seaweed beds in other regions, appear to preferentially use seagrass beds in the Menai Bay area, as previously reported from other areas in the region (Lugendo et al 2005; Gullström et al 2008). The study illustrates that seaweed beds and seagrass meadows, while both being important juvenile habitats for fish in the shallow seascape around Zanzibar, still have their own separate roles to fill.
Paper III shows that the abundance, biomass and taxon richness of mobile epifauna can be high in tropical seaweed beds, and that they exceeded those of closely situated seagrass meadows, with the two habitats harbouring differing epifaunal communities. The observed difference in abundance mainly stems from a higher abundance of crustaceans (mainly amphipods) in seaweed beds, while the difference in taxon richness stems from more numerous taxa of decapod crustaceans and gastropods. Small crustaceans, such as amphipods, are commonly regarded as important food sources for many invertivorous fish species (Brook 1977; Choat and Kingett 1982; Edgar and Shaw 1995). As the abundance of invertivorous fish is also higher in seaweed beds, this suggests that the higher abundance of epifauna in
31 seaweed beds is not due to a lower predation pressure, but rather indicates that seaweed beds may act as feeding grounds for invertivorous fish.
Potential to utilize native strains in seaweed farming Due to the spread of introduced seaweeds discovered in Paper I, as well as the increased productivity problems of seaweed farms in East Africa, it was of great interest to assess whether native eucheumoids could be used for farming purposes. Paper IV shows, however, that the growth rate of introduced SEA Eucheuma denticulatum exceeds that of the native EA E. denticulatum and Kappaphycus alvarezii in two out of three farm sites in Zanzibar. Also when compared on a haplotype level, the EA haplotype PAC5 had a lower growth rate than the SEA haplotype E13, and additionally also a higher epiphyte cover. Unfortunately, PAC5 was the only EA haplotype present in sufficient numbers to enable comparisons on a haplotype level, and while two other EA haplotypes were present in the cultivations, their performance could not be evaluated. Regarding the potential to farm native EA seaweeds, it is important to remember that the seaweeds brought in from SEA have undergone a long continuous strain selection before being brought to Zanzibar, whereas no such selection has occurred for the native strains.
The finding that introduced SEA E. denticulatum can have a higher growth rate than its native EA congener, may provide it with a competitive advantage in a natural setting, and could potentially be one of the reasons for the relative success in attaining the high frequency found in natural seaweed beds (Paper I), but this must be explored further. Results for the SEA E. denticulatum in this study, in combination with previous studies performed in the EA region, paints a picture of decreasing growth rates, which illustrates the productivity problems that have been reported for the region (Msuya 2011a; Msuya and Porter 2014).
SYNTHESIS This thesis shows that a cryptic invasion of natural seaweed beds has taken place in Zanzibar, as they now contain more non-indigenous than native Eucheuma denticulatum. On the one hand this thesis illustrates that the spread of farmed haplotypes has not led to a complete domination of shallow seaweed beds by the introduced haplotypes of E. denticulatum, as the seaweed beds where the SEA haplotypes are the dominant eucheumoids are currently not dominated by E. denticulatum. Rather, the seaweed beds in the study area still contain relatively similar percentages of the other large seaweed species, such as Sargassum and Turbinaria, compared to the
32 estimations for the area in the 1970’s (Mshigeni 1984). On the other hand this thesis also contributes to the knowledge that introduced eucheumoids can become established in a new environment, as has also been shown in e.g. Hawaii, India and Panama (Conklin and Smith 2005; Chandrasekaran et al 2008; Sellers et al 2015). Seaweeds that are introduced for farming purposes commonly have high growth rates and vegetative propagation, and while such traits make them easy and profitable to cultivate, the same traits have also been suggested to be common in seaweeds that become invasive (Andreakis and Schaffelke 2012), and may hence aid the introduced seaweeds in spreading and becoming established in their new surroundings. Although it should be noted that a species that becomes invasive in one area must not necessarily become invasive in all areas where it is introduced (Trowbridge 2006), the growing body of knowledge showing that seaweed species introduced for farming purposes can become both established and invasive should be further taken into account before any introductions are made.
In addition to this, the thesis gives indications of decline of natural populations of eucheumoid species in Zanzibar, as compared to the scarce data available from the area (Mshigeni 1984). Two of the eucheumoid species identified from the region, Kappaphycus alvarezii and E. platycladum, appears to have a very low frequency of occurrence and to have disappeared from areas where they used to be found. The most common eucheumoid species, E. denticulatum, is still present in natural seaweed beds to a larger extent. However, as it appears to reproduce mainly by vegetative means, this could lead to a limited potential for the species to adapt to changing environmental conditions. There are indications that also in mainland Tanzania eucheumoid species are disappearing from areas where they historically have been abundant (Mshigeni 1979; pers. obs.), and some areas previously found to have rich algal assemblages are now essentially bare (A. Buriyo pers. comm.; pers. obs.), but the reasons for this are unknown.
In the light of the current changes to seaweed assemblages the results from the investigations on the ecological contribution of seaweed beds to the tropical seascape are of high importance. This thesis illustrates that tropical seaweed beds can have a high species and taxon richness of not only macrophytes, but also of mobile epifauna and fish, indicating that seaweed beds can be of importance for local species diversity. The results also suggest that seaweed beds act as juvenile and feeding grounds to a number of fish species, and as habitats to numerous invertebrates, and additionally that these species and taxa may differ from other vegetated habitats. Therefore it is important to recognize seaweed beds as a separate part of the tropical seascape. Studies showing that connectivity within a complex
33 tropical seascape may influence the abundance and diversity of fish through diel and ontogenetic migrations are gaining ground (see e.g. Olds et al 2012b; Berkström et al 2012; Martin et al 2015), and connectivity within the seascape is increasingly being considered for management actions (Olds et al 2012b; Olds et al 2014). However, studies of tropical seascape connectivity do commonly not include seaweed beds, even though the results from this thesis, as well as studies from other tropical regions show that seaweed beds can act as juvenile fish habitats in many different areas of the tropical world (Wilson et al 2010; Chaves et al 2013; Evans et al 2014). This indicates a need for including seaweed beds in future studies of seascape connectivity and management actions. To attain a more complete view of the utilization of the shallow tropical seascape, more focus should be put on habitats that previously have received little attention, as they may provide important ecosystem services, although not yet recognized.
The productivity problems that are being experienced by the seaweed farming communities, not only in East Africa but also in other regions of eucheumoid farming (Hayashi et al 2010; Msuya 2011a; Msuya and Porter 2014; Hurtado et al 2015), illustrates the need for diversification of cultivars if a sustainable cultivation is to be secured. This thesis, as well as a previous study by Halling et al. (2013), indicates that the current cultivation of E. denticulatum in Zanzibar is based solely on one introduced SEA haplotype. This heavy reliance on such a narrow genetic basis could be hazardous, as it has been suggested that it may increase the vulnerability to both biotic and abiotic stressors (Guillemin et al 2008; Loureiro et al 2015). While this thesis illustrates that the introduced SEA E. denticulatum has a higher growth rate than the EA E. denticulatum and K. alvarezii, it is important to consider that no selection of cultivars have so far been performed for the native EA eucheumoids. A total of six native EA haplotypes have so far been discovered (Zuccarello et al 2006; Halling et al 2013; Tano et al 2015 (Paper I); unpubl. data), which illustrates that there may be potential for future strain selection. However, as most of the EA haplotypes appear to have low frequency of occurrence around Zanzibar, and as it is currently not possible to visually separate EA and SEA E. denticulatum in the field, this indicates that future strain selection may be a demanding endeavour.
FUTURE RESEARCH This thesis has aimed to add to the body of knowledge concerning tropical seaweed beds and the spread of non-native haplotypes, yet much remains to be done to explore the ecology of tropical seaweed beds, as well as to understand the potential implications of the spread of non-native haplotypes. Further studies should for example explore if there are similar patterns of
34 decreasing abundance of eucheumoids also on a larger scale in the East African region, as there are indications that this may be the case. Additionally, it should be investigated if the spread of non-indigenous Eucheuma denticulatum from seaweed farms is also taking place in other areas of East Africa, as seaweed farming of SEA haplotypes is occurring in mainland Tanzania, as well as Mafia Island, Kenya, Madagascar and Mozambique. There are indications that spread of SEA E. denticulatum and Kappaphycus alvarezii is occurring in mainland Tanzania (Tano et al. unpubl. data), although the extent of this is unknown. The potential of non- indigenous strains to become nuisances in other habitats should also be further studied, as an overgrown coral reef has recently been discovered in the Menai Bay area (Fig. 6), and preliminary data indicates that the culprit is the non-indigenous SEA E. denticulatum haplotype E13 (Eggertsen et al. unpubl. data).
Figure 6. Eucheuma denticulatum growing on an Acropora coral reef.
An important aspect to further explore in regards to the ecology of tropical seaweed beds is the potential seasonality of seaweed assemblages in East Africa. As it is known that tropical algal assemblages may differ in biomass, cover and species composition on a seasonal basis (Trono and Lluisma 1990; Vuki and Price 1994; Ateweberhan et al 2005; Wilson et al 2014), it would be of interest to explore the seasonal changes in East African seaweed beds, and to evaluate how this affects the associated biota.
35
Regarding the potential for farming native eucheumoids there are several aspects that should be explored. Apart from strain selection of EA eucheumoids for higher growth rates, the carrageenan quantity and quality are important components to address, as a higher quality and/or quantity could compensate for lower growth rates.
36 POPULÄRVETENSKAPLIG SAMMANFATTNING Makroalger (tång) har under en lång tid använts av människor för såväl mat som foder och gödning, och de har skördats från algbäddar och samlats på stränderna efter att ha blåst i land. I takt med att användningsområdena har ökat, och ohållbart skördande har lett till en minskning av naturliga algresurser, så har algodling blivit allt vanligare.
Eucheumoider utgör ett av de algsläkten vars produktion har ökat mycket under de sista årtiondena, som odlas för utvinning av karragen, ett stabiliseringsmedel som används i t.ex. mejeriprodukter och kosmetika. De algarter som används mest i odling har två olika utbredningsområden, ett i Sydostasien och ett i östra Afrika. Under 1970-talet påbörjades odling av dessa alger efter att skördarna från de naturliga algbäddarna minskade drastiskt. Odlingen startade i Filippinerna, men har därefter brett ut sig även över andra delar av tropikerna, och i dagsläget har Sydostasiatiska alger blivit introducerade till mer än 30 länder i odlingssyfte. Att introducera främmande arter innebär en risk för spridning utanför odlingen, och att de kan etablera sig i det vilda i det nya området, där den kan förändra de ekologiska förutsättningarna för inhemska arter.
På Zanzibar i östra Afrika introducerades de sydostasiatiska algerna 1989, och odlingen av en av arterna, Eucheuma denticulatum, ökade snabbt. Inte förrän långt senare blev det klarlagt att de afrikanska och de sydostasiatiska algerna, trots att de är samma art, är genetiskt distinkta. Detta innebär i princip att det finns liknande risker som om man hade introducerat en helt ny art, eftersom det är möjligt att de skiljer sig åt i t.ex. hur snabbt de växer och hur mycket de blir betade av växtätande djur. Undersökningar visade att de sydostasiatiska algerna hade spritt sig från algodlingarna. Att undersöka utbredningen och omfattningen av de introducerade algerna i jämförelse med de inhemska var därför ett av avhandlingens syften.
Resultaten visade att de inhemska algerna har blivit sällsynta, och att även i områden där det aldrig har funnits några odlingar så hittas nu mest de sydostasiatiska algerna. Vi såg också att de inhemska algerna förefaller att huvudsakligen föröka sig vegetativt. Detta innebär att de förökar sig genom att delar av algen bryts av, lossnar och förs bort med vattenrörelser, där de avbrutna delarna har kapacitet att börja växa om de hittar ett lämpligt underlag att fästa vid. Ur en evolutionär synvinkel kan detta vara problematiskt, eftersom detta riskerar att leda till få en liten genetisk variation, och en bred genetisk variation kan vara viktigt för att en art ska kunna anpassa sig till en omgivning som förändras. Utöver detta visade det
37 sig att vissa av de arter av eucheumoider som funnits i området tidigare nu är ovanliga, och på vissa platser verkade de ha försvunnit helt.
Dessa resultat, i kombination med att det finns uppgifter om att alger verkar minska i Tanzania, ledde vidare till frågan om vilka ekologiska funktioner tropiska algbäddar faktiskt har. Många andra tropiska habitat har undersökts i ganska stor utsträckning, och det är känt att t.ex. sjögräsängar och mangroveskogar är viktiga områden för juvenila fiskar, framförallt av korallrevsarter och arter som är viktiga för fisket. Betydelsen av algområden i tropikerna är däremot ganska okänd, och även om några få studier visat att de kan vara viktiga på andra håll i världen, så var ingenting känt om deras betydelse i Östafrika. Vi valde därför att undersöka vilka fiskar, och i vilka ålderklasser, som använde sig av algområdena, och jämförde det med sjögräsängar i närheten. Våra resultat visade att algområden i Östafrika har ett högt antal av juvenila fiskar, och framförallt ett högt antal av korallrevsarter och arter viktiga för det lokala fisket. I jämförelse med sjögräsängar, som är kända för att vara viktiga för ung fisk, visade det sig att algområden faktiskt hade ett högre antal juvenila fiskar. Vi undersökte också antalet ryggradslösa djur (evertebrater), och fann att algområden hade stort antal av evertebrater och även ett högt antal fiskar som äter evertebrater. Detta förefaller alltså innebära att algområden inte bara kan vara viktiga för ung fisk, utan även har möjlighet att fungera som födosöksområden.
Vår sista studie tog oss tillbaka till starten igen: Algodlingen. Under senare år har algodlingen börjat gå sämre i både Östafrika och Sydostasien, och det har visat sig att det kan vara riskabelt att basera en hel odling på bara några få kloner eftersom det kan öka risken för sjukdomar. På Zanzibar såg vi redan i vår första studie att all odling baseras på mer eller mindre en enda klon (individer med samma ursprung och identisk genuppsättning), vilket kan leda till att produktionen kan minska dramatiskt om omgivningarna, t.ex. vattentemperaturen, förändras. För att få in nya alger i odlingarna finns det två alternativ, antingen introduceras nya alger från Sydostasien, eller så kan man försöka odla de inhemska algerna. Vi ville undersöka om detta var möjligt, och odlade därför alger från naturliga algområden för att kunna jämföra de Östafrikanska algerna med de Sydostasiatiska som används i odlingarna. Våra resultat visade att de sydostasiatiska algerna växer snabbare, men visade också att det finns ett antal olika inhemska alger att testa om man vill försöka selektera fram alger som växer snabbare. I dagsläget har det hittats sex olika inhemska genetiska varianter av arten E. denticulatum, och trots att det kan vara tidskrävande att försöka ta fram inhemska alger med en bra tillväxt, så är det en möjlighet som borde utvecklas i framtiden.
38 ACKNOWLEDGEMENTS To paraphrase John Donne: No woman is an island. This thesis could not have come into existence without the avid support of a great many people, and some people in particular. Johan Tano, during this whole time you have been nothing but supportive, and I cannot express how grateful I am for all your help, both in the field and at home. I couldn’t have done it without you! Maria Eggertsen, you have been my main partner in crime for a number of years now, and I can honestly say that it has been nothing but a pleasure! Our collaboration has been a great inspiration, continuously resulting in new ideas. I also really appreciate that you are as interested as me in identifying fish and creepy-crawlies- it makes me feel way less weird. I sincerely hope that I can be of as much help to you during your PhD-project as you have been to me. I would like to thank my supervisors, Christina Halling and Sofia Wikström, for their great support during my time as a PhD-student. Though you, like me, were fairly new to working in East Africa at the start of the project, I would like to think that we’ve all learnt a lot together, and I greatly appreciate you giving me this opportunity. I would also like to thank Amelia Buriyo, who has been our local guiding hand and provided us with valuable insights into the region. To the most wonderful of genetic work mentors, Josefine Larsson and Emma Lind, I would like to say thank you for all your patience, and all your genuine interest and efforts in how to best homogenize a seaweed that’s sturdy enough to be used in construction. Josefin Sagerman, thanks for helping me improve the kappa, and thank you even more for being a fellow algae enthusiast. Charlotte Berkström, you have been a great help in writing the fish and epifauna papers! To the amazing people Serena Donadi, Anni Golz and Elisa Alonso-Aller I would like to offer my greatest gratitude for the endless statistical discussions, beautiful graphs, mental support and dinners with lots of cheese. I might have been a bit preoccupied lately, but I’m done now, so – Let’s go for beers! Ndevu, asante sana kwa wewe kusaidia mimi kila miaka hii, ninashukuru. I would also like to thank the personnel at IMS for their help during my work in Zanzibar, especially Narriman Jiddawi for assisting in all sorts of practical things and one of my co-authors Flower Msuya for seaweed farm guiding and assistance. Additionally I would like to thank Johan Eklöf and Nils Kautsky for their help in transforming this work from mere papers into a thesis during the internal review. Last but not least I would like to thank my family for many marine themed travels (and all my diving certificates...) that have led me down this path, and a special thanks go to mormor Gunhild Runemark: tack för alla somrar på Malkvarn med dig och morfar. Att få plaska runt i Östersjön var troligen en av de upplevelser som ledde mig hit. Trots att jag, ironiskt nog, tyckte att tången var lite rälig att gå i.
39 And while I’m at it, I would like to recommend to anyone who is feeling stressed and overworked at times to get a dog. Skilla, you have no idea how much help you’ve been in keeping me sane.
Financial support The studies were funded by the Swedish Research Council and Sida (SWE2010-052).
LITERATURE CITED Able KW, Hagan SM (2000) Effects of common reed (Phragmites australis) invasion on marsh surface macrofauna: Response of fishes and decapod crustaceans. Estuaries 23:633–646. Alonso Aller E, Gullström M, Eveleens Maarse FKJ, et al (2014) Single and joint effects of regional- and local-scale variables on tropical seagrass fish assemblages. Mar Biol. doi: 10.1007/s00227-014-2514-7 Andreakis N, Schaffelke B (2012) Invasive marine seaweeds: Pest or prize? In: Wiencke C, Bischof K (eds) Seaweed Biol. Springer Berlin Heidelberg, Berlin, Heidelberg, pp 235–262 Ask EI (2003) Creating a sustainable commercial Eucheuma cultivation industry: the importance and necessity of the human factor. 17th Int. Seaweed Sym. Cape Town, South Africa. pp 13–18 Ask EI, Azanza R V (2002) Advances in cultivation technology of commercial eucheumatoid species: a review with suggestions for future research. Aquaculture 206:257–277. Ask EI, Batibasaga A, Zertuche-González JA, de San M (2003a) Three decades of Kappaphycus alvarezii (Rhodophyta) introduction to non-endemic locations. Int. Seaweed Symp. 17. pp 49–57 Ask EI, Ledua E, Batibasaga A, Mario S (2003b) Developing the cottonii (Kappaphycus alvarezii) cultivation industry in the Fiji Islands. In: Chapman A, Anderson R, Vreeland V, Davison I (eds) Proc. XVIIth Int. Seaweed Symp. Oxford University Press, pp 81–85 Ateweberhan M, Bruggemann JH, Breeman AM (2005) Seasonal dynamics of Sargassum ilicifolium (Phaeophyta) on a shallow reef flat in the southern Red Sea (Eritrea). Mar Ecol Prog Ser 292:159–171. doi: 10.3354/meps292159 Baamonde López S, Baspino Fernández I, Barreiro Lozano R, Cremades Ugarte J (2007) Is the cryptic alien seaweed Ulva pertusa (Ulvales, Chlorophyta) widely distributed along European Atlantic coasts? Bot Mar 50:267–274. doi: 10.1515/BOT.2007.030 Barrios J, Bolaños J, López R (2007) Blanqueamiento de arrecifes coralinos por la invasion de Kappaphycus alvarezii (Rhodophyta) en Isla Cubagua, estado Nueva Esparta, Venezuela. Bol Inst Ocean Venez 46:147–152. Benoit LK, Askins RA (1999) Impact of the spread of Phragmites on the distribution of birds in Connecticut tidal marshes. Wetlands 19:194–208.
40 Berkström C, Gullström M, Lindborg R, et al (2012) Exploring “knowns” and “unknowns” in tropical seascape connectivity with insights from East African coral reefs. Estuar Coast Shelf Sci 107:1–21. doi: 10.1016/j.ecss.2012.03.020 Berkström C, Lindborg R, Thyresson M, Gullström M (2013b) Assessing connectivity in a tropical embayment: Fish migrations and seascape ecology. Biol Conserv 166:43–53. doi: 10.1016/j.biocon.2013.06.013Berkström C, Jörgensen T, Hellström M (2013a) Ecological connectivity and niche differentiation between two closely related fish species in the mangrove- seagrass-coral reef continuum. Mar Ecol Prog Ser 477:201–215. doi: 10.3354/meps10171 Bixler HJ, Porse H (2011) A decade of change in the seaweed hydrocolloids industry. J Appl Phycol 23:321–335. doi: 10.1007/s10811-010-9529-3 Brook IM (1977) Trophic relationships in a seagrass community (Thalassia testudinum), in Card Sound, Florida. Fish diets in relation to macrobenthic and cryptic faunal abundance. Trans Am Fish Soc 106:219–229. doi: 10.1577/1548- 8659(1977)106<219:TRIASC>2.0.CO;2 Bryceson I (2002) Coastal aquaculture developments in Tanzania: Sustainable and non-sustainable experiences. West Indian Ocean J Mar Sci 1:1–10. Bulboa C, de Paula EJ, Chow F (2008) Germination and survival of tetraspores of Kappaphycus alvarezii var. alvarezii (Solieriaceae, Rhodophyta) introduced in subtropical waters of Brazil. Phycol Res 56:39–45. doi: 10.1111/j.1440- 1835.2008.00483.x Bulboa CR, de Paula EJ (2005) Introduction of non-native species of Kappaphycus (Rhodophyta, Gigartinales) in subtropical waters: Comparative analysis of growth rates of Kappaphycus alvarezii and Kappaphycus striatum in vitro and in the sea in south-eastern Brazil. Phycol Res 53:183–188. Buschmann AH, Correa JA, Westermeier R, et al (2001) Red algal farming in Chile: a review. Aquaculture 194:203–220. Carr MH (1994) Effects of macroalgal dynamics on recruitment of a temperate reef fish. Ecology 75:1320–1333. Castelar B, Reis RP, Moura AL, Kirk R (2009) Invasive potential of Kappaphycus alvarezii off the south coast of Rio de Janeiro state, Brazil: a contribution to environmentally secure cultivation in the tropics. Bot Mar 52:283–289. doi: 10.1515/BOT.2009.002 Chambers RM, Meyerson LA, Saltonstall K (1999) Expansion of Phragmites australis into tidal wetlands of North America. Aquat Bot 64:261–273. doi: 10.1016/S0304-3770(99)00055-8 Chandrasekaran S, Nagendran NA, Pandiaraja D, et al (2008) Bioinvasion of Kappaphycus alvarezii on corals in the Gulf of Mannar, India. Curr Sci 94:1167–1172. Chaves LTC, Pereira PHC, Fetosa JLL (2013) Coral reef fish association with macroalgal beds on a tropical reef system in North-eastern Brazil. Mar Freshw Res. doi: http://dx.doi.org/10.1071/MF13054 Choat JH, Kingett PD (1982) The influence of fish predation on the abundance cycles of an algal turf invertebrate fauna. Oecologia 54:88–95. Chopin T, Buschmann AH, Halling C, et al (2001) Integrating seaweeds into marine aquaculture systems: a key toward sustainability. J Phycol 37:975–986. Christie H, Jörgensen NM, Norderhaug KM, Waage-Nielsen E (2003) Species distribution and habitat exploitation of fauna associated with kelp (Laminaria hyperborea) along the Norwegian Coast. J Mar Biol Assoc UK 83:687–699. doi: 10.1017/S0025315403007653h
41 Christie H, Norderhaug KM, Fredriksen S (2009) Macrophytes as habitat for fauna. Mar Ecol Prog Ser 396:221–233. doi: 10.3354/meps08351 Chuang S-H (1977) Ecology of Singapore and Malayan coral reefs - preliminary classification. Proc. 3rd Int. Coral Reef Symp. pp 55–61 Chung IK, Beardall J, Mehta S, et al (2011) Using marine macroalgae for carbon sequestration: a critical appraisal. J Appl Phycol 23:877–886. doi: 10.1007/s10811-010-9604-9 Chung IK, Oak JH, Lee J a., et al (2013) Installing kelp forests/seaweed beds for mitigation and adaptation against global warming: Korean Project Overview. ICES J Mar Sci 70:1038–1044. doi: 10.1093/icesjms/fss206 Conklin EJ, Smith JE (2005) Abundance and spread of the invasive red algae, Kappaphycus spp., in Kane’ohe Bay, Hawai’i and an experimental assessment of management options. Biol Invasions 7:1029–1039. Costa O., Attrill M., Pedrini A., De-Paula J. (2000) Benthic macroalgal distribution in coastal and offshore reefs at Porto Seguro Bay, Brazilian Discovery Coast. Proc 9th Int Coral Reef Symp 1:499–507. Cox TE, Smith CM (2011) Thermal ecology on an exposed algal reef: Infrared imagery a rapid tool to survey temperature at local spatial scales. Coral Reefs 30:1109–1120. doi: 10.1007/s00338-011-0799-2 Dahl AL (1973) Benthic algal ecology in a deep reef and sand habitat off Puerto Rico. Bot Mar 16:171–175. doi: 10.1515/botm.1973.16.3.171 de la Torre-Castro M, Lyimo TJ (eds) (2012) People, nature and research in Chwaka Bay, Zanzibar, Tanzania. WIOMSA, Zanzibar Town Diaz-Pulido G, Gouezo M, Tilbrook B, et al (2011) High CO2 enhances the competitive strength of seaweeds over corals. Ecol Lett 14:156–162. doi: 10.1111/j.1461-0248.2010.01565.x Doty MS (1987) The production and use of Eucheuma. In: Doty M, Caddy J, Santelices B (eds) Case Stud. seven Commer. seaweed Resour., FAO Fisher. FAO, Rome, pp 123–161 Doty MS, Santos GA (1978) Carrageenans from tetrasporic and cystocarpic Eucheuma species. Aquat Bot 4:143–149. Duffy JE (1990) Amphipods on seaweeds: Partners or pests? Oecoligia 83:267–276. Duggins DO, Simenstad CA, Estes JA (1989) Magnification of secondary production by kelp detritus in coastal marine ecosystems. Science (80- ) 245:170–173. Dunton KH (2001) δ15N and δ13C measurements of Antarctic Peninsula fauna: trophic relationships and assimilation of benthic seaweeds. Am Zool 41:99–112. doi: 10.1668/0003-1569(2001)041[0099:NACMOA]2.0.CO;2 Edgar GJ, Shaw C (1995) The production and trophic ecology of shallow-water fish assemblages in southern Australia II. Diets of fishes and trophic relationships between fishes and benthos at Western Port, Victoria. J Exp Mar Bio Ecol 194:83–106. doi: 10.1016/0022-0981(95)00084-4 Eklöf JS, de la Torre Castro M, Adelsköld L, et al (2005) Differences in macrofaunal and seagrass assemblages in seagrass beds with and without seaweed farms. Estuar Coast Shelf Sci 63:385–396. doi: 10.1016/j.ecss.2004.11.014 Eklöf JS, Henriksson R, Kautsky N (2006a) Effects of tropical open-water seaweed farming on seagrass ecosystem structure and function. Mar Ecol Prog Ser 325:73–84. Eklöf JS, Torre-Castro M De, Nilsson C, Rönnbäck P (2006b) How do seaweed farms influence local fishery catches in a seagrass-dominated setting in Chwaka Bay, Zanzibar? Aquat Living Resour 19:137–147. doi: 10.1051/alr
42 Evans RD, Wilson SK, Field SN, Moore JAY (2014) Importance of macroalgal fields as coral reef fish nursery habitat in north-west Australia. Mar Biol 161:599–607. doi: 10.1007/s00227-013-2362-x FAO (2014) The State of World Fisheries and Aquaculture 2014. Rome Feitosa JLL, Ferreira BP (2015) Distribution and feeding patterns of juvenile parrotfish on algal-dominated coral reefs. Mar Ecol 36:462–474. doi: 10.1111/maec.12154 Ferreira LEC, Oliveira Junqueira Ribeiro A De, Villac MC, Lopes RM (2009) Marine bioinvasions in the Brazilian coast: brief report on history of events, vectors, ecology, impacts and management of non-indigenous species. In: Rilov G, Crooks JA (eds) Biol. Invasions Mar. Ecosyst., Ecological. Springer-Verlag, Berlin Heidelberg, pp 459–477 Fox RJ, Bellwood DR (2007) Quantifying herbivory across a coral reef depth gradient. Mar Ecol Prog Ser 339:49–59. doi: 10.3354/meps339049 Fredriksen S, Christie H, Andre Sæthre B (2005) Species richness in macroalgae and macrofauna assemblages on Fucus serratus L. (Phaeophyceae) and Zostera marina L. (Angiospermae) in Skagerrak, Norway. Mar Biol Res 1:2–19. doi: 10.1080/17451000510018953 Fulton CJ, Depczynski M, Holmes TH, et al (2014) Sea temperature shapes seasonal fluctuations in seaweed biomass within the Ningaloo coral reef ecosystem. Limnol Oceanogr 59:156–166. doi: 10.4319/lo.2014.59.01.0156 Gepp A, Gepp ES (1908) Marine algae (Chlorophyceae and Phaeophyceae) and marine phanerogams of the “Sealark” Expedition, collected by J Stanley Gardiner. Trans Linn Soc LONDON 2ND Ser Zool 12:373–398. Gestoso I, Olabarria C, Troncoso JS (2010) Variability of epifaunal assemblages associated with native and invasive macroalgae. Mar Freshw Res 61:724. doi: 10.1071/MF09251 Guillemin M-L, Faugeron S, Destombe C, et al (2008) Genetic variation in wild and cultivated populations of the haploid-diploid red alga Gracilaria chilensis: How farming practices favor asexual reproduction and heterozygosity. Evolution (N Y) 62:1500–1519. doi: 10.1111/j.1558-5646.2008.00373.x Gullström M, Bodin M, Nilsson PG, Öhman MC (2008) Seagrass structural complexity and landscape configuration as determinants of tropical fish assemblage composition. Mar Ecol Prog Ser 363:241–255. doi: 10.3354/meps07427 Halling C, Wikström SA, Lilliesköld-Sjöö G, et al (2013) Introduction of Asian strains and low genetic variation in farmed seaweeds: indications for new management practices. J Appl Phycol 25:89–95. Hay ME, Colburn T, Downing D (1983) Spatial and temporal patterns in herbivory on a Caribbean fringing reef: the effects on plant distribution. Oecologia 58:299–308. Hayashi L, Hurtado AQ, Msuya FE, et al (2010) A review of Kappaphycus farming: Prospects and constraints. In: Israel A, Einav R, Seckbach J (eds) Seaweeds their Role Glob. Chang. Environ. Springer, Heidelberg Longon New York, pp 255–283 Hill NAO, Rowcliffe JM, Koldewey HJ, Milner-Gulland EJ (2012) The interaction between seaweed farming as an alternative occupation and fisher numbers in the central Philippines. Conserv Biol 26:324–334. doi: 10.1111/j.1523- 1739.2011.01796.x Hughes TP, Rodrigues MJ, Bellwood DR, et al (2007) Phase shifts, herbivory, and the resilience of coral reefs to climate change. Curr Biol 17:360–365. doi: 10.1016/j.cub.2006.12.049
43 Huo Y, Wu H, Chai Z, et al (2012) Bioremediation efficiency of Gracilaria verrucosa for an integrated multi-trophic aquaculture system with Pseudosciaena crocea in Xiangshan harbor, China. Aquaculture 326-329:99– 105. doi: 10.1016/j.aquaculture.2011.11.002 Hurtado AQ, Neish IC, Critchley AT (2015) Developments in production technology of Kappaphycus in the Philippines: more than four decades of farming. J Appl Phycol 27:1945–1961. doi: 10.1007/s10811-014-0510-4 Isaac WE (1960) Marine botany of the kenya coast 1. A first list of Kenya marine algae. J East Africa Nat Hist Soc 26:75–83. Isaac WE (1967) Marine botany of the Kenya coast 2. A second list of Kenya marine algae. J East Africa Nat Hist Soc 27:1–6. Isaac WME, Isaac FM (1968) Marine botany of the Kenya coast 3. General account of the environment flora and vegetation. J East Africa Nat Hist Soc Natl Museum 27:7–28. Jessen C, Wild C (2013) Herbivory effects on benthic algal composition and growth on a coral reef flat in the Egyptian Red Sea. Mar Ecol Prog Ser 476:9–21. doi: 10.3354/meps10157 Johnstone RW, Muhando CA, Francis J (1998) The status of the coral reefs of Zanzibar: one example of a regional predicament. Ambio 27:700–707. Johnstone RW, Olafsson E (1995) Some environmental aspects of open water algal cultivation: Zanzibar, Tanzania. Ambio 24:465–469. Jones GP (1984) Population ecology of the temperate reef fish Pseudolabrus celidotus Bloch and Scheneider (Pisces: Labridae). I. Factors influencing recruitment. J Exp Mar Bio Ecol 75:257–276. Jones S (1958) Economic seaweeds. Krann S, Guiry MD (2000) Strain selection in the edible brown seaweed Alaria esculenta: Genetic fingerprinting and hybridization studies under laboratory conditions. Mar Resour Ser 8:1–30. Kwak SN, Klumpp DW (2004) Temporal variation in species composition and abundance of fish and decapods of a tropical seagrass bed in Cockle Bay, North Queensland, Australia. Aquat Bot 78:119–134. doi: 10.1016/j.aquabot.2003.09.009 Largo DB, Fukami K, Nishijima T, Ohno M (1995) Laboratory-induced development of the ice-ice disease of the farmed red algae Kappaphycus alvarezii and Eucheuma denticulatum (Solieriaceae, Gigartinales, Rhodophyta). J Appl Phycol 7:539–543. doi: 10.1007/BF00003940 Lawson GW (1969) Some observations on the littoral ecology of rocky shores in East Africa (Kenya and Tanzania). Trans R Soc South Africa 38:329–339. doi: 10.1080/00359196909519096 Lenanton R, Robertson A, Hansen J (1982) Nearshore accumulations of detached macrophytes as nursery areas for fish. Mar Ecol Prog Ser 9:51–57. doi: 10.3354/meps009051 Levin PS, Hay ME (1996) Responses of temperate reef fishes to alterations in algal structure and species composition. Mar Ecol Prog Ser 134:37–47. Levy I, Friedlander M (1990) Strain selection in Gracilaria spp. Bot Mar 33:339– 345. Lirasan T, Twide P (1993) Farming Eucheuma in Zanzibar, Tanzania. Hydrobiologia 260-261:353–355. Lluisma AO, Ragan MA (1995) Relationships among Eucheuma denticulatum, Eucheuma isiforme and Kappaphycus alvarezii (Gigartinales, Rhodophyta) based on nuclear ssu-rRNA gene sequences. J Appl Phycol 7:471–477. doi: 10.1007/BF00003931
44 Lobban CS, Harrison PJ (1997) Seaweed ecology and physiology. Cambridge University Press, Cambridge, UK Loureiro R, Gachon CMM, Rebours C (2015) Seaweed cultivation: potential and challenges of crop domestication at an unprecedented pace. New Phytol 206:489–492. doi: 10.1111/nph.13278 Lugendo BR, Nagelkerken I, Van Der Velde G, Mgaya YD (2006) The importance of mangroves, mud and sand flats, and seagrass beds as feeding areas for juvenile fishes in Chwaka Bay, Zanzibar: Gut content and stable isotope analyses. J Fish Biol 69:1639–1661. doi: 10.1111/j.1095-8649.2006.01231.x Lugendo BR, Pronker A, Cornelissen I, et al (2005) Habitat utilisation by juveniles of commercially important fish species in a marine embayment in Zanzibar , Tanzania. 158:149–158. doi: 10.1051/alr Lyimo TJ, Mvungi EF, Mgaya YD (2008) Abundance and diversity of seagrass and macrofauna in the intertidal areas with and without seaweed farming. Tanzanian J Sci 34:41–52. Lüning K, Pang S (2003) Mass cultivation of seaweeds: current aspects and approaches. J Appl Phycol 15:115–119. doi: 10.1023/A:1023807503255 Løvstad Holdt S, Kraan S (2011) Bioactive compounds in seaweed: Functional food applications and legislation. J Appl Phycol 23:543–597. doi: 10.1007/s10811- 010-9632-5 Mallea AJA, Villanueva FCA, Bernardi J, Cabrera R (2014) Ecological risk assessment of the introduction of exotic carrageenophytes in the tropical Western Atlantic. J Appl Phycol 26:2055–2063. doi: 10.1007/s10811-014-0385- 4 Martin TSH, Olds AD, Pitt KA, et al (2015) Effective protection of fish on inshore coral reefs depends on the scale of mangrove-reef connectivity. Mar Ecol Prog Ser 527:157–165. doi: 10.3354/meps11295 Matanjun P, Mohamed S, Mustapha NM, Muhammad K (2009) Nutrient content of tropical edible seaweeds, Eucheuma cottonii, Caulerpa lentillifera and Sargassum polycystum. J Appl Phycol 21:75–80. doi: 10.1007/s10811-008- 9326-4 McClanahan TR (1988) Seasonality in East Africa’s coastal waters. Mar Ecol Prog Ser 44:191–199. McClanahan TR, Muthiga NA, Kamukuru AT, et al (1999) The effects of marine parks and fishing on coral reefs of northern Tanzania. Biol Conserv 89:161–182. McCook LJ (1997) Effects of herbivory on zonation of Sargassum spp. within fringing reefs of the central Great Barrier Reef. Mar Biol 129:713–722. doi: 10.1007/s002270050214 McIvor L, Maggs CA, Provan J, Stanhope MJ (2001) rbcL sequences reveal multiple cryptic introductions of the Japanese red alga Polysiphonia harveyi. Mol Ecol 10:911–919. doi: 10.1046/j.1365-294X.2001.01240.x McManus JW, Polsenberg JF (2004) Coral–algal phase shifts on coral reefs: Ecological and environmental aspects. Prog Oceanogr 60:263–279. doi: 10.1016/j.pocean.2004.02.014 Mollion J, Braud J-P (1993) A Eucheuma (Solieriaceae, Rhodophyta) cultivation test on the south-west coast of Madagascar. Hydrobiologia 260-261:373–378. Morrissey J (1980) Community structure and zonation of microalgae and hermatypic corals on a fringing reef flat of magnetic island (Queensland, Australia). Aquat Bot 8:91–139. doi: 10.1016/0304-3770(80)90045-5 Mshigeni KE (1984) The red algal genus Eucheuma (Gigartinales, Solieriaceae) in East Africa: An underexploited resource. Hydrobiologia 116-117:347–350.
45 Mshigeni KE (1973) Exploitation of seaweeds in Tanzania. Tanzan Notes Rec 72:19–36. Mshigeni KE (1979) The economic algal genus Eucheuma (Rhodophyta, Gigartinales): Observations on the morphology and distribution ecology of Tanzanian species. Bot Mar XXII:437–445. doi: 10.1515/botm.1979.22.7.437 Msuya FE (2011a) Environmental changes and their impact on seaweed farming in Tanzania. World Aquac 42:34–37. Msuya FE (2011b) The impact of seaweed farming on the socioeconomic status of coastal communities in Zanzibar, Tanzania. World Aquac 42:45–48. Msuya FE, Buriyo A, Omar I, et al (2014) Cultivation and utilisation of red seaweeds in the Western Indian Ocean (WIO) Region. J Appl Phycol 26:699– 705. doi: 10.1007/s10811-013-0086-4 Msuya FE, Porter M (2014) Impact of environmental changes on farmed seaweed and farmers: the case of Songo Songo Island, Tanzania. J Appl Phycol 26:2135– 2141. doi: 10.1007/s10811-014-0243-4 NBS (2014) Basic demographic and socio-economic profile, Tanzania Zanzibar. Dar es Salaam, Tanzania Neish AC, Shacklock F, Fox CH, Simpson ANDFJ (1977) The cultivation of Chondrus crispus. Factors affecting growth under greenhouse conditions. Can J Bot 55:2263–2271. Neori A, Chopin T, Troell M, et al (2004) Integrated aquaculture: rationale, evolution and state of the art emphasizing seaweed biofiltration in modern mariculture. Aquaculture 231:361–391. doi: 10.1016/j.aquaculture.2003.11.015 Norambuena R (1996) Recent trends of seaweed production in Chile. Hydrobiologia 326/327:371–379. doi: 10.1007/BF00047834 Norderhaug KM, Christie H, Fosså JH, Fredriksen S (2005) Fish–macrofauna interactions in a kelp (Laminaria hyperborea) forest. J Mar Biol Assoc UK 85:1279–1286. doi: 10.1017/S0025315405012439 Olds AD, Connolly RM, Pitt K a., Maxwell PS (2012a) Habitat connectivity improves reserve performance. Conserv Lett 5:56–63. doi: 10.1111/j.1755- 263X.2011.00204.x Olds AD, Pitt K a., Maxwell PS, Connolly RM (2012b) Synergistic effects of reserves and connectivity on ecological resilience. J Appl Ecol 49:1195–1203. doi: 10.1111/jpe.12002 Olds AD, Connolly RM, Pitt KA, et al (2014) Incorporating surrogate species and seascape connectivity to improve marine conservation outcomes. Conserv Biol 28:982–991. doi: 10.1111/cobi.12242 Pang T, Liu J, Liu Q, et al (2015) Observations on pests and diseases affecting a eucheumatoid farm in China. J Appl Phycol 27:1975–1984. doi: 10.1007/s10811-014-0507-z Parker HS (1974) The culture of the red algal genus Eucheuma in the Philippines. Aquaculture 3:425–439. Pettersson-Löfquist P (1995) The development of open-water algae farming in Zanzibar: Reflections on the socioeconomic impact. Ambio 24:487–491. Pickering T (2006) Advances in seaweed aquaculture among Pacific Island countries. J Appl Phycol 18:227–234. doi: 10.1007/s10811-006-9022-1 Pickering TD, Skelton P, Sulu RJ (2007) Intentional introductions of commercially harvested alien seaweeds. Bot Mar 50:338–350. doi: 10.1515/BOT.2007.039 Provan J, Booth D, Todd NP, et al (2007) Tracking biological invasions in space and time: elucidating the invasive history of the green alga Codium fragile using old DNA. Divers Distrib 14:343–354. doi: 10.1111/j.1472-4642.2007.00420.x
46 Radulovich R, Umanzor S, Cabrera R, Mata R (2015) Tropical seaweeds for human food, their cultivation and its effect on biodiversity enrichment. Aquaculture 436:40–46. doi: http://dx.doi.org/10.1016/j.aquaculture.2014.10.032 Randall JE (1961) Overgrazing of algae by herbivorous marine fishes. Ecology 42:812. Rao MU (1973) The seaweed potential of the seas around India. Proc. Symp. Living Resour. Seas India. pp 687–692 Rasher DB, Hay ME (2010) Chemically rich seaweeds poison corals when not controlled by herbivores. Proc Natl Acad Sci U S A 107:9683–8. doi: 10.1073/pnas.0912095107 Russell DJ (1983) Ecology of the imported red seaweed Eucheuma striatum Schmitz on Coconut Island, Oahu, Hawaii. Pacific Sci 37:87–107. Sahoo D, Elangbam G, Devi SS (2012) Using algae for carbon dioxide capture and bio-fuel production to combat climate change. Phykos 42:32–38. Saltonstall K (2002) Cryptic invasion by a non-native genotype of the common reed, Phragmites australis, into North America. Proc Natl Acad Sci U S A 99:2445– 2449. doi: 10.1073/pnas.032477999 Samoilys MA, Carlos G (2000) Determining methods of underwater visual census for estimating the abundance of coral reef fishes. Environ Biol Fishes 57:289– 304. Schaffelke B, Hewitt CL (2007) Impacts of introduced seaweeds. Bot Mar 50:397– 417. doi: 10.1515/BOT.2007.044 Schmidt A, Coll M, Romanuk T, Lotze H (2011) Ecosystem structure and services in eelgrass Zostera marina and rockweed Ascophyllum nodosum habitats. Mar Ecol Prog Ser 437:51–68. doi: 10.3354/meps09276 Sellers AJ, Saltonstall K, Davidson TM (2015) The introduced alga Kappaphycus alvarezii (Doty ex P. C. Silva, 1996) in abandoned cultivation sites in Bocas del Toro, Panama. BioInvasions Rec 4:1–7. doi: 10.3391/bir.2015.4.1.01 Sen S (1991) Seaweed collection and culture in Tanzania. FAO, ALCOM field document GCP/INT/436/SWE.14, Harare, Zimbabwe Sievanen L, Crawford B, Pollnac R, Lowe C (2005) Weeding through assumptions of livelihood approaches in ICM: Seaweed farming in the Philippines and Indonesia. Ocean Coast Manag 48:297–313. doi: 10.1016/j.ocecoaman.2005.04.015 Smit AJ (2004) Medicinal and pharmaceutical uses of seaweed natural products: A review. J Appl Phycol 16:245–262. Smith JE, Hunter CL, Smith CM (2002) Distribution and reproductive characteristics of nonindigenous and invasive marine algae in the Hawaiian Islands. Pacific Sci 56:299–315. doi: 10.1353/psc.2002.0030 Solgaard Thomsen M, Deluqui Gurgel CF, Fredericq S, McGlathery KJ (2006) Gracilaria vermiculophylla (Rhodophyta, Gracilariales) in Hog Island Bay, Virginia: a cryptic alien and invasive macroalga and taxonomic correction. J Phycol 42:139–141. doi: 10.1111/j.1529-8817.2005.00160.x Stanley N (1987) Production, properties and uses of carrageenan. Prod. Util. Prod. from Commer. seaweeds Stål J, Pihl L, Wennhage H (2007) Food utilisation by coastal fish assemblages in rocky and soft bottoms on the Swedish west coast: Inference for identification of essential fish habitats. Estuar Coast Shelf Sci 71:593–607. doi: 10.1016/j.ecss.2006.09.008 Tanner JE (1995) Competition between scleractinian corals and macroalgae: An experimental investigation of coral growth, survival and reproduction. J Exp Mar Bio Ecol 190:151–168. doi: 10.1016/0022-0981(95)00027-O
47 Tano S, Halling C, Lind E, et al (2015) Extensive spread of farmed seaweeds causes a shift from native to non-native haplotypes in natural seaweed beds. Mar Biol 162:1983–1992. doi: 10.1007/s00227-015-2724-7 Taylor JD (1968) Coral reef and associated invertebraet communities (mainly Molluscan) around Mahe, Seychelles. Philos Trans R Soc B Biol Sci 254:129– 206. Titlyanov EA, Titlyanova T V (2010) Seaweed cultivation: Methods and problems. Russ J Mar Biol 36:227–242. doi: 10.1134/S1063074010040012 Tobey J, Torell E (2006) Coastal poverty and MPA management in mainland Tanzania and Zanzibar. Ocean Coast Manag 49:834–854. doi: 10.1016/j.ocecoaman.2006.08.002 Tobisson E, Andersson J, Ngazi Z, et al (1998) Local knowledge and practice in Chwaka Bay, Zanzibar. Ambio 27:677–685. Troell M, Halling C, Nilsson A, et al (1997) Integrated marine cultivation of Gracilaria chilensis (Gracilariales, Rhodophyta) and salmon cages for reduced environmental impact and increased economic output. Aquaculture 156:45–61. doi: 10.1016/S0044-8486(97)00080-X Trono GC, Lluisma A (1990) Seasonality of standing crop of a Sargassum (Fucales, Phaeophyta) bed in Bolinao, Pangasinan, Philippines. Hydrobiologia 204/205:331–338. Trowbridge CD (2006) A global proliferation of non-native marine and brackish macroalgae. Seaweed Resour. Tsai CC, Wong SL, Chang JS, et al (2004) Macroalgal assemblage structure on a coral reef in Nanwan Bay in southern Taiwan. Bot Mar 47:439–453. doi: 10.1515/BOT.2004.061 Tsuda RT (1977) Zonational patterns of the phaeophyta (brown algae) on Guam’s fringing reefs. Third Int. Coral Reef Symp. pp 371–375 Tyler EHM, Manica A, Jiddawi N, Speight MR (2011) A role for partially protected areas on coral reefs: Maintaining fish diversity? Aquat Conserv Mar Freshw Ecosyst 21:231–238. doi: 10.1002/aqc.1182 Untawale AG, Jagtap TG (1989) Observations on marine macrophytes of the Republic of Seychelles. Bot Mar 32:115–120. doi: 10.1515/botm.1989.32.2.115 Vairappan CS, Chung CS, Hurtado AQ, et al (2008) Distribution and symptoms of epiphyte infection in major carrageenophyte-producing farms. J Appl Phycol 20:477–483. Wakibia JG, Bolton JJ, Keats DW, Raitt LM (2006) Factors influencing the growth rates of three commercial eucheumoids at coastal sites in Southern Kenya. J Appl Phycol 18:565–573. Valderrama D, Cai J, Hishamunda N, et al (2015) The economics of Kappaphycus seaweed cultivation in developing countries: a comparative analysis of farming systems. Aquac Econ Manag 19:251–277. doi: 10.1080/13657305.2015.1024348 Valderrama D, Cai J, Hishamunda N, Ridler N (eds) (2013) Social and economic dimensions of carrageenan seaweed farming. Fish Aquac Tech Pap 580:204. Wanders JBW (1976) The role of benthic algae in the shallow reef of Curacao (Netherlands Antilles) II: Primary productivity of the Sargassum beds on the North-East coast submarine plateau. Aquat Bot 2:327–335. doi: 10.1017/CBO9781107415324.004 Varma RP, Rao KK (1962) Algal resources of Pamban area. Indian J Fish 9A:205– 211. Vasquez EA, Glenn EP, Brown JJ, et al (2005) Salt tolerance underlies the cryptic invasion of North American salt marshes by an introduced haplotype of the
48 common reed Phragmites australis (Poaceae). Mar Ecol Prog Ser 298:1–8. doi: 10.3354/meps298001 Wernberg T, Vanderklift MA, How J, Lavery PS (2006) Export of detached macroalgae from reefs to adjacent seagrass beds. Oecologia 147:692–701. doi: 10.1007/s00442-005-0318-7 Viejo RM (1999) Mobile epifauna inhabiting the invasive Sargassum muticum and two local seaweeds in northern Spain. Aquat Bot 64:131–149. doi: 10.1016/S0304-3770(99)00011-X Wiencke C, Bischof K (eds) (2012) Seaweed biology. Springer-Verlag, Berlin Heidelberg Willi Y, Van Buskirk J, Hoffmann AA (2006) Limits to the adaptive potential of small populations. Annu Rev Ecol Evol Syst 37:433–458. Williams SL, Smith JE (2007) A global review of the distribution, taxonomy, and impacts of introduced seaweeds. Annu Rev Ecol Evol Syst 38:327–359. doi: 10.1146/annurev.ecolsys.38.091206.095543 Wilson SK, Depczynski M, Fisher R, et al (2010) Habitat associations of juvenile fish at Ningaloo Reef, Western Australia: the importance of coral and algae. PLoS One 5:e15185. doi: 10.1371/journal.pone.0015185 Wilson SK, Fulton CJ, Depczynski M, et al (2014) Seasonal changes in habitat structure underpin shifts in macroalgae-associated tropical fish communities. Mar Biol 161:2597–2607. doi: 10.1007/s00227-014-2531-6 Wismer S, Hoey AS, Bellwood DR (2009) Cross-shelf benthic community structure on the Great Barrier Reef: Relationships between macroalgal cover and herbivore biomass. Mar Ecol Prog Ser 376:45–54. doi: 10.3354/meps07790 Vuki VC, Price IR (1994) Seasonal changes in the Sargassum populations on a fringing coral reef, Magnetic Island, Great Barrier Reef region, Australia. Aquat Bot 48:153–166. doi: 10.1016/0304-3770(94)90082-5 Yamada H, Nanami A, Ohta I, et al (2012) Occurrence and distribution during the post-settlement stage of two Choerodon species in shallow waters around Ishigaki Island, southern Japan. Fish Sci 78:809–818. doi: 10.1007/s12562-012- 0506-4 Yarish C, Wamukoya G (1990) Seaweeds of potential economic importance in Kenya: field survey and future prospects. Hydrobiologia 204/205:339–346. Zaneveld JS (1959) The utilization of marine algae in tropical South and East Asia. Econ Bot 13:89–131. Zemke-White WL, Smith JE (2006) Environmental impacts of seaweed farming in the tropics. In: Critchley AT, Ohno M, Largo D (eds) World Seaweed Resour. ETI BioInformatics, Univ. Amsterdam (CD-ROM series), Wokingham, pp 1–42 Zubia M, Robledo D, Freile-Pelegrin Y (2007) Antioxidant activities in tropical marine macroalgae from the Yucatan Peninsula, Mexico. J Appl Phycol 19:449– 458. doi: 10.1007/s10811-006-9152-5 Zuccarello GC, Critchley AT, Smith J, et al (2006) Systematics and genetic variation in commercial shape Kappaphycus and Eucheuma (Solieriaceae, Rhodophyta). J Appl Phycol 18:643–651. Zuccarello GC, Lokhorst GM (2005) Molecular phylogeny of the genus Tribonema (Xanthophyceae) using rbcL gene sequence data: monophyly of morphologically simple algal species. Phycologia 44:384–392. Zuccarello GC, West JA, Kamiya M, King RJ (1999) A rapid method to score plastid haplotypes in red seaweeds and its use in determining parental inheritance of plastids in the red alga Bostrychia (Ceramiales). Hydrobiologia 401:207–214.
49