Marine flora of the Iles Eparses (Scattered Islands): A longitudinal transect through the Mozambique Channel

Acta Oecologica 72 (2016) 33e40

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Original article

Marine flora of the Iles Eparses (Scattered Islands): A longitudinal transect through the Mozambique Channel L. Mattio a, b, *, M. Zubia c, G.W. Maneveldt d, R.J. Anderson a, e, J.J. Bolton a, C. de Gaillande c, O. De Clerck f, C.E. Payri g a

Department of Biological Sciences and Marine Research Institute, University of Cape Town, 7701 Rondebosch, South Africa School of Plant Biology and Oceans Institute, University of Western Australia, WA6009 Perth, Australia UMR Ecosyst
emes Insulaires Oc eaniens, Universit e de Polyn esie française, 98702 Faa'a, Tahiti, French Polynesia d Department of Biodiversity and Conservation Biology, University of the Western Cape, Bellville 7535, South Africa e Department of Agriculture, Forestry and Fisheries, Private Bag X2, Roggebaai, 8012, South Africa f Phycology Research Group, Ghent University, 9000 Ghent, Belgium g UMR ENTROPIE, LabEx-CORAIL, Institut de Recherche pour le D eveloppement, 98848 Noum ea, New Caledonia b c

a r t i c l e i n f o

a b s t r a c t

Article history: Received 13 February 2015 Received in revised form 3 August 2015 Accepted 1 September 2015 Available online 14 September 2015

The diversity of marine macrophytes of small islands in the South Western Indian Ocean region has been poorly documented and little or no information is available for the Iles Eparses (or Scattered Islands) in the Mozambique Channel. We present the first species checklist for the three largest islands of the Iles Eparses: Europa, Juan de Nova and Glorioso. Overall, with a total of 321 marine macrophyte species recorded (incl. 56% Rhodophyta, 27% Chlorophyta, 15% Phaeophyceae and 2% Magnoliophyta; Europa: 134 spp., Juan de Nova: 157 spp. and Glorioso: 170 spp.) these islands harbour 23.5% of the total species recorded for the Mozambique Channel region. We report 36 new records for the Mozambique Channel including 29 undescribed new and cryptic species. Our results highlight a decrease in species richness southward in the Channel. Because of their longitudinal arrangement between the northern and the southern ends of the Channel and their central position, Europa, Juan de Nova and Glorioso Islands represent data points of particular biogeographical interest and could be critical ‘stepping stones’ for connectivity in the highly dynamic Mozambique Channel region. © 2015 Elsevier Masson SAS. All rights reserved.

Keywords: Biogeography Connectivity Diversity Macroalgae Seagrasses Western Indian Ocean

1. Introduction The diversity of marine macrophytes in the South Western Indian Ocean (SWIO) is mainly known from scattered checklists and regional taxonomic publications for Madagascar, Mauritius, union, and the Seychelles (e.g. Børgesen, Mozambique, Re 1940e1957; Bornet, 1885; Carvalho and Bandeira, 2003; Coppejans et al., 2004; Critchley et al., 1997; De Clerck et al., 2004; Hariot, 1902; Massingue and Bandeira, 2007; Mshigeni, 1985; Payri, 1985; Rabesandratana, 1988; Wynne, 1995) while four illustrated books focus on sections of the African East coast in Kenya, Tanzania and South Africa (Jaasund, 1976; De Clerck et al., 2005; Moorjani and Simpson, 1988; Oliveira et al., 2005). All

* Corresponding author. School of Plant Biology and Oceans Institute, The University of Western Australia, WA6009 Perth, Australia. E-mail address: [email protected] (L. Mattio). http://dx.doi.org/10.1016/j.actao.2015.09.001 1146-609X/© 2015 Elsevier Masson SAS. All rights reserved.

literature records prior to 1996 have been comprehensively listed by Silva et al. (1996), but further unpublished data are available for the region (e.g. Madagascar: Douternlungne, 2003; Farghaly, 1980). Most of these texts deal exclusively with marine macroalgae (seaweeds), with some including macroscopic cyanobacteria and/or marine angiosperms (seagrasses). The marine floras of the islands in the Mozambique Channel remain poorly understood; for example, Algaebase (Guiry and Guiry, 2015) records only 59 spp. for the Comoros (incl. Mayotte) and no published species lists are available for the Iles Eparses (Scattered Islands). The Iles Eparses are a group of five uninhabited islands and reefs administered by France, on behalf the French Southern and Antarctic Lands (TAFF: Terres Australes et Antartiques françaises), which despite the visits of several botanists from the middle of the 19th century (http://ileseparses.cbnm.org/index.php/histoire-dela-botanique, accessed 20/01/2015), seem to have been avoided by phycologists, although a few scattered collections appear in local reports.

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L. Mattio et al. / Acta Oecologica 72 (2016) 33e40

The three largest islands of the Iles Eparses: Europa, Juan de Nova and Glorioso, are spread across 10
of latitude between the southern and the northern ends of the Mozambique Channel (Fig. 1). The other two are Bassas da India, a reef emersed only at low tide just north of Europa, and Tromelin, a tiny island (less than foue €t et al., 2008) with very limited terrestrial 1 km2, (Andre vegetation, north-east of Madagascar. The Mozambique Channel is of particular interest from a biogeographical perspective as it is affected by a combination of complex currents and mesoscale eddies (Quartly and Srokosz, 2004; Halo et al., 2014; Hancke et al., 2014), which have been put forward as vectors of unique patterns of distribution and connectivity (Gopal et al., 2006; Marsac et al., 2014; Obura, 2012; Reddy et al., 2014; Tew Kai and Marsac, 2010). A study on reef-building corals (Obura, 2012) shows evidence for a high diversity region in the northern section of the Mozambique Channel, decreasing southward with increasing eddyeshelf interactions and upwelling from the South Madagascar Plateau, resulting in a transition to colder/higher nutrient fauna and habitats. Obura (2012) suggested that patterns observed for corals may be similar for other shallow marine taxa. Due to the longitudinal arrangement of the Iles Eparses in the Mozambique Channel, the shallow marine biodiversity of Europa, Juan de Nova and Glorioso may be expected to follow the same trend. Due to their isolation, the Iles Eparses are subject to very limited human disturbance. Nevertheless, Juan de Nova and Glorioso are situated in the ‘Western Madagascar marine ecoregion’ (considered vulnerable) and one of 22 global ‘Tropical coral’ ecoregions considered most critical for global conservation (Olson and Dinerstein, 2002). The fauna and flora of the archipelago are protected by the TAAF and enforcement is maintained by a permanent military detachment on each of the three main islands. Although the anthropogenic influence is strictly controlled, there are anecdotal reports of illegal visits by foreign fishermen. There are also invasive populations of cats and goats and relics of attempted colonisation on some islands. With the aim of providing baseline

Fig. 1. Geographical position of Europa, Juan de Nova and Glorioso Islands in the Mozambique Channel.

studies for registering these islands as Marine Protected Areas , Ressources et Con(MPAs), the BIORECIE program (Biodiversite cifs Coralliens des Iles Eparses), led by the French servation des Re veloppement (IRD) was funded for Institut de Recherche pour le De a period of three years (2011e2013). As part of this program, during three intensive SCUBA diving and snorkelling-based field expeditions the first significant marine macrophyte reference collections were made for the Iles Eparses. The present study aims to fill a gap in our knowledge of the marine flora (including macroalgae and seagrasses) of the Iles Eparses, to provide a baseline species checklist for future biogeographical studies and management purposes, and to conduct a preliminary investigation of diversity patterns between the three largest islands: Europa, Juan de Nova and Glorioso. 2. Material & methods 2.1. Sites and sample collection Europa is the southernmost island in the Mozambique Channel, located 550 km east of southern Mozambique and 300 km west of southern Madagascar (22
2105900 S, 40
220 0600 E, Fig. 1). It is the largest island (31.63 km2 land surface area) of the Iles Eparses with a roughly circular shape of 6e7 km diameter. It is surrounded by sand dunes and fringing reefs, with a maximum elevation of 7 m. The shallow lagoon is almost empty at low tide and half of its surface is occupied by mangroves. Reefs and lagoon area account for a total of 17.5 km2. The Island of Juan de Nova is situated about 400 km north of Europa, about 100 km west of Madagascar and 200 km east of Mozambique (17
0301900 S, 42
430 2400 E, Fig. 1). It is a small island (5.48 km2 land surface area), measuring 6 km at its longest end and 1.6 km at its narrowest end. Sand dunes reach up to 12 m high. The island is surrounded by a large lagoon and fringing reefs which together cover 206.69 km2. The Glorioso archipelago represents the northernmost islands of the Mozambique Channel. It is located about 140 km north-west of the northern tip of Madagascar and about 170 and 500 km north east of Mayotte (Comoros) and Juan de Nova respectively, and 460 km east of the northern tip of Mozambique (11
340 4400 S, 47
170 2800 E, Fig. 1). The archipelago is composed of two main islands: Grande Glorieuse, the largest, which is 2.3 km at its widest section, and Ile du Lys, which is only 600 m long. The two islands are separated by 10 km of shallow reefs and are surrounded by a lagoon and reefs (196.56 km2 total area) (surface areas are from foue €t et al., 2008); for more information on the Scattered Andre Islands see also http://ileseparses.cbnm.org/ and http://www.taaf. fr/-District-des-iles-Eparses). Samples were collected from a total of 17 sites at Europa (December 2011), 26 sites at Glorioso (December 2012) and 27 sites at Juan de Nova (December 2013). All collections were thus made in the Austral summer. Sites were chosen based primarily on satellite images in order to represent as many of the different habitats found foue €t et al., 2015 in this issue) from around those islands (see Andre the intertidal down to about 20 m deep, and taking into account logistic difficulties. At each site, sampling effort was 60 min and all different species encountered were collected. Samples were sorted, photographed, given preliminary identifications and pressed the same day. At least two specimens of each species found at each island were processed to form a principal and a duplicate voucher collection. The principal voucher collection of Europa was deposum National d’Histoire Naturelle ited in the Herbarium of the Muse (PC) in Paris, France with duplicates in the Herbarium of the Uni de la Re union (REU), France. Voucher collections for Juan de versite Nova and Glorioso Islands will also be deposited in these Herbaria.

L. Mattio et al. / Acta Oecologica 72 (2016) 33e40

Non-geniculate corallines were deposited in the Herbarium of the University of the Western Cape (UWC) in South Africa. Herbarium abbreviations follow Thiers (2015). Subsamples were stored in buffered formaldehyde in seawater (3%) for later microscope examination and in silica gel or ethanol for later DNA analyses. Tissue collections are available upon request to the authors.

35

Kwazulu-Natal region (Northeast coast, South Africa) was obtained from the personal database of R.J. Anderson, J.J. Bolton and from Maneveldt et al. (2008). 3. Results 3.1. Species diversity

2.2. Species identification Detailed morphological and anatomical examinations and final identifications were carried out during two workshops involving the authors of the present paper. The first workshop, focussing on the material collected at Europa, was held at the University of Cape Town, Cape Town, South Africa in June 2011 (J.J. Bolton, G.W. Maneveldt, R.J, Anderson, O. De Clerck, L. Mattio and M. Zubia). The second, focussing on collections from the remaining two islands veloppement in was held at the Institut de Recherche pour le De a, New Caledonia in December 2014 (C.E. Payri, L. Mattio and Noume M. Zubia). Voucher specimens from selected groups were further examined, and DNA analyses processed when possible, by authors of the present paper or through existing collaborations as follows: Rhodophyta e Laurencia complex and Chondria: C. Francis (University of Cape Town, South Africa); Nemaliales: S.-M. Lin (National Taiwan Ocean University, Taiwan) and S.-L. Liu (Tunghai University, Taiwan); Hypnea: V. Johnson (University of Cape Town, South Africa); Corallines: G.W. Maneveldt (University of the Western Cape, South Africa); Asparagopsis: L. Dijoux (IRD, New Caledonia). Chlorophyta e Halimeda and Codium: C.E. Payri (IRD, New Caledonia) and H. Verbruggen (University of Melbourne, Australia); Caulerpa: W. Prud’Homme van Reine (Netherlands), C.E. Payri, J. Roessger and L. Millet (IRD, New Caledonia); other Cladophorales: F. Leliaert (Ghent University, Belgium); Ulvales: F. Mineur (Queen's University of Belfast, Ireland), C.E. Payri and L. Lagourgue (IRD, New Caledonia). Phaeophyceae e Dictyota: O. De Clerck (Ghent University, Belgium); Lobophora: C. Vieira (IRD, New Caledonia/Ghent University, Belgium); Padina: C.E. Payri (IRD, New Caledonia); Sargassaceae: L. Mattio (University of Cape Town, South Africa/University of Western Australia, Australia). 2.3. Additional analyses Species accumulation curves were calculated separately for each of the three islands. This method performs a random draw of n sites and calculates the cumulative species richness from the number of sites. The species accumulation curve provides an estimation of the cumulative species richness according to the sampling effort. It was built using random resampling (Gotelli and Colwell, 2001) without replacement, on 200 random permutations using the “specaccum” function of the vegan package of the software R (R Development Core Team, 2013). To compare species richness across islands an asymptotic richness estimator, the Chao index, was used. This method is used for extrapolating species diversity out to the (presumed) asymptote and calculates the “expected number of species” depending on the number of rare species. The Chao index was calculated using the “Chao2” function of the fossil package of the software R (R Development Core Team, 2013). For regional comparisons, species lists were assembled for countries and islands bordering the Mozambique Channel. Records available for Madagascar, the Seychelles, the Comoros, Tanzania, and Mozambique were downloaded from Algaebase (Guiry and Guiry, 2015), which is considered to provide the most comprehensive species checklist for the region. A list of species in the

A total of 394 specimens were collected and processed for Europa, 381 for Juan de Nova and 466 for Glorioso Island. After the workshops, a total of 321 morphotaxa were identified for the three islands (Europa: 134, Juan de Nova: 157 and Glorioso: 170), representing overall proportions of 56% Rhodophyta, 27% Chlorophyta, 15% Phaeophyceae and 2% Magnoliophyta. Table 1 provides a summary of the species richness per taxonomic group and island. About 38% of all morphotaxa were positively identified (Rhodophyta 32%, Chlorophyta 54%, Phaeophyceae 40% and Magnoliophyta 100%). The rest await final confirmation, mainly because they require DNA analyses (e.g. Hypnea, Chondria) or represent cryptic diversity (e.g. Portieria, Lobophora). A substantial portion of the corallines could not be identified because the material was vegetative and lacked the necessary reproductive features. At least 29 taxa (9%) represent undescribed species new to science (2) (e.g. Rhodopeltis sp. and Gibsmithia sp.) or cryptic taxa (27) (e.g. Dictyota, Lobophora), and 36 taxa (11%) represent new records for the area. A checklist for the three islands is provided in Appendix A.1. Species accumulation curves (Fig. 2) do not approach an asymptote for the number of sites investigated for any of the three islands, indicating that many more species could be collected if the sampling effort could be increased. The Chao values provided estimates of: 507 species for Glorioso, 569 for Juan de Nova and 624 for Europa. These values are significantly greater than the numbers of species sampled. 3.2. Species geographical distribution The species list compiled for the comparison of regional records is provided in Appendix A.2. A summary of the results is presented in Table 2. Between the three islands, the floras of Glorioso and Juan de Nova were the most similar with 79 spp. in common while Europa shared 54 spp. with Glorioso and 42 spp. with Juan de Nova. A total of only 35 species (about 11%) were common to all three islands and included mostly species common to the region (e.g. Actinotrichia fragilis (Forsskål) Børgesen, Caulerpa serrulata (Forsskål) Weber-van Bosse, Dichotomaria marginata (J. Ellis & Solander) Lamarck, Gelidiella acerosa (Forsskål) Feldmann & G. Hamel, Porolithon onkodes (Heydrich) Foslie, Rhipidosiphon javensis Montagne and Turbinaria ornata (Turner) J. Agardh). On a regional basis, although sampling and taxonomic effort was not similar in all localities, results showed that the richest marine flora is documented for Tanzania and Kwazulu-Natal (Table 2), followed by the Seychelles and Madagascar. The highest similarities for the three islands were found with the marine flora of Tanzania. 4. Discussion 4.1. The marine flora of the Iles Eparses We identified and listed a total of 322 species: 134 from Europa, 157 from Juan de Nova and 170 from Glorioso. Among the 321 species, 11% (36 spp.) were new records for the Mozambique Channel area, and a further 9% (29 spp.) were either new to science (2 spp.) or cryptic species (27 spp., possibly endemic). The Dictyotaceae was the richest family observed at all three islands, with a total of 38 taxa represented mainly by species from

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L. Mattio et al. / Acta Oecologica 72 (2016) 33e40

Table 1 Summary of species richness per taxonomic group for Europa (EUR), Juan de Nova (JDN) and Glorioso (GLO).

Order: Bryopsidales Family: Bryopsidaceae Family: Caulerpaceae Family: Codiaceae Family: Dichotomosiphonaceae Family: Halimedaceae Family: Rhipiliaceae Family: Udoteaceae Order: Cladophorales Family: Anadyomenaceae Family: Cladophoraceae Family: Pithophoraceae Family: Siphonocladaceae Family: Valoniaceae Order: Dasycladales Family: Dasycladaceae Family: Polyphysaceae Order: Ulvales Family: Ulvaceae Phyllum: Chlorophyta % of total macrophytes Order: Dictyotales Family: Dictyotaceae Order: Ectocarpales Family: Acinetosporaceae Family: Scytosiphonaceae Order: Fucales Family: Sargassaceae Order: Ralfsiales Family: Ralfsiaceae Order: Sphacelariales Family: Sphacelariaceae Phyllum: Ochrophyta % of total macrophytes Order: Acrosymphytales Family: Acrosymphytaceae Order: Bonnemaisoniales Family: Bonnemaisoniaceae Order: Ceramiales Family: Callithamniaceae Family: Ceramiaceae Family: Dasyaceae Family: Delesseriaceae Family: Rhodomelaceae Family: Spyridiaceae Family: Wrangeliaceae Order: Corallinales Family: Corallinaceae Order: Hapalidiales Family: Hapalidiaceae Order: Gelidiales Family: Gelidiaceae Family: Gelidiellaceae Family: Pterocladiaceae Order: Gigartinales Family: Corynocystaceae Family: Cystocloniaceae Family: Chondrymeniaceae Family: Dumontiaceae Family: Kallymeniaceae Family: Phacelocarpaceae Family: Phyllophoraceae Family: Rhizophyllidaceae Family: Solieriaceae Family: incertae sedis Order: Gracilariales Family: Gracilariaceae Order: Halymeniales Family: Halymeniaceae Order: Nemaliales Family: Galaxauraceae

EUR

JDN

GLO

Total

15 3 5 2 1 1 1 2 11 2 1 1 4 3 1 1 1 2 2

33 2 16 0 1 8 2 4 13 2 2 2 5 2 2 2 0 0 0

32 1 15 0 1 10 0 5 18 2 2 2 8 4 3 2 1 1 1

55 6 24 2 1 12 3 7 25 4 5 2 10 4 5 3 2 2 2

30 22%

48 31%

54 32%

87 27%

18 18 2 1 1 1 1 2 2 1 1

16 16 1 0 1 3 3 1 1 0 0

16 16 2 1 1 4 4 0 0 1 1

38 38 2 1 1 4 4 3 3 1 1

23 17%

25 16%

23 13%

48 15%

0 0 1 1 23 0 1 3 3 13 1 2 14 14 1 1 5 1 3 1 9 1 6 1 1 0 0 0 0 0 0 0 0 1 1 6 4

1 1 1 1 27 4 4 3 5 8 1 2 14 14 0 0 2 0 1 1 17 0 7 0 3 0 1 1 2 2 1 1 1 2 2 8 5

2 2 1 1 30 5 1 4 3 15 0 2 14 14 1 1 2 0 1 1 10 0 4 0 3 1 0 0 1 0 1 1 1 5 5 10 3

2 2 1 1 56 5 6 6 8 26 2 3 30 30 2 2 6 1 3 2 29 1 14 1 5 1 1 1 2 2 1 1 1 7 7 16 6

Table 1 (continued ) EUR

JDN

GLO

2 1 1 0 6 6 0 0 10 4 1 1 4

3 3 1 2 1 1 0 0 7 2 0 2 3

7 1 1 0 6 6 1 1 5 2 0 1 2

10 3 1 2 10 10 1 1 18 8 1 3 6

77 58%

84 52%

89 52%

182 56%

Order: Alismatales Family: Cymodoceaceae Family: Hydrocharitaceae

4 2 2

1 1 0

5 3 2

5 3 2

Phyllum: Magnoliophyta % of total macrophytes

4 3%

1 1%

5 3%

5 2%

134

157

170

321

Family: Liagoraceae Order: Nemastomatales Family: Nemastomataceae Family: Schizymeniaceae Order: Peyssonneliales Family: Peyssonneliaceae Order: Rhodogorgonales Family: Rhodogorgonaceae Order: Rhodymeniales Family: Champiaceae Family: Hymenocladiaceae Family: Lomentariaceae Family: Rhodymeniaceae Phyllum: Rhodophyta % of total macrophytes

Total macrophytes

Total

Fig. 2. Species accumulation curves for Europa, Juan de Nova and Glorioso.

the genera Dictyota and Lobophora. The Bryopsidales were also relatively well represented, and particularly conspicuous at Juan de Nova and Glorioso where species from the genera Caulerpa and Halimeda were very abundant and diverse (24 and 12 taxa, respectively). On these latter two islands, calcified Halimeda segments appeared to be an important component of sand, while only one species was collected from Europa. The Rhodomelaceae and the Corallinaceae were the richest families of the Rhodophyta and appeared well represented at all three islands. The seagrasses were abundant and diverse at Europa and Glorioso, whereas they were very rare at Juan de Nova where only a very small patch of Thalassodendron ciliatum (Forsskål) den Hartog was found. Only Europa had populations of Ulva cf. flexuosa Wulfen occurring in brackish water holes on the island, and it also had large populations of Amphisbetema indica (J.Agardh) Weber-van Bosse and Wrangelia spp. in the intertidal. Europa was also the only island of the three investigated where the genus Codium was present. Of the coralline red algae, except for two specimens belonging to the Hapalidiales (Nelson et al., 2015), the entire collection was dominated by species of the order Corallinales. No members of the Sporolithales were found. Porolithon onkodes was the most abundant species collected, followed by Neogoniolithon cf. brassicaflorida (Harvey) Setchell & L.R. Mason. This finding is not surprising as Maneveldt and Keats (2014) have reported P. onkodes to be comparatively widespread throughout the tropical and subtropical Indo-Pacific and Atlantic Oceans. Neogoniolithon brassica-florida is

L. Mattio et al. / Acta Oecologica 72 (2016) 33e40

37

Table 2 Total number of species documented for countries and islands bordering the Mozambique Channel, number of species shared with Europa (EUR), Juan de Nova (JDN) and Glorioso (GLO). The full dataset is available in Appendix A.2 and was compiled from Guiry and Guiry (2015), Maneveldt et al. (2008), R.J. Anderson and J.J Bolton unpublished database of South African macrophytes, and results from the present study.

Total spp. spp. shared with EUR spp. shared with JDN spp. shared with GLO

Europa Juan de Nova

Glorioso Comoros and Mayotte

KZN, south Africa

Madagascar Mozambique Seychelles Tanzania (incl. Zanzibar)

Mozambique Channel

134 134

157 42

170 54

59 9

504 39

340 36

226 26

431 43

505 56

1368 134

42

157

79

14

50

48

31

55

71

157

54

79

170

13

46

42

30

52

65

170

similarly widely reported (Guiry and Guiry, 2015). The present study represents the most south-western records (previously the Aldabra Islands) of Porolithon gardineri (Foslie) Foslie and Porolithon craspedium (Foslie) Foslie for the Indian Ocean. Our species accumulation curves and results of the Chao Index indicated that many more species could be added to the list if sampling effort was increased. All three islands were sampled during the month of December and down to depths of 15e20 m but over a limited period. Repeated collections at different seasons and investigation at greater depths would likely capture more taxa. The Sargassaceae may be cited as an example. Species from this group were inconspicuous in December at all islands, while large quantities of Turbinaria spp. and Sargassum spp. were sighted in winter at Europa (P. Chabanet, pers. com.), suggesting that more species may occur than the one recorded here. Besides seasonal species, a number of cryptic species probably still await discovery and, despite the taxonomic effort dedicated to the identification of the present collections (two workshops, and at least 17 specialists), only about 38% of all morphotypes were positively identified (32% for Rhodophyta, 54% for Chlorophyta, 40% for Phaeophyceae and 100% for Magnoliophyta), because for some groups identification at species level was not possible without molecular analysis. Noteworthy examples include species complexes such as Halymenia ndez-Kantún et al., 2012), durvillei Bory de Saint-Vincent (Herna Portieria hornemanii (Lyngbye) P.C. Silva (De Clerck et al., 2012; Payo et al., 2013), Lobophora variegata (J.V. Lamouroux) Womersley ex E.C. Oliveira (Vieira et al., 2014) or Gibsmithia hawaiiensis Doty (Gabriel et al., 2013) and members of the Laurenciae, Liagoraceae, Hypneaceae, Peyssonneliaceae, Dictyotaceae, Cystocloniaceae, as well as a number of Bryopsidales, to name only a few. 4.2. Regional distribution The distribution of the marine macrophyte species richness in the Mozambique Channel (Table 2) supports the biogeographic pattern documented by Obura (2012) for reef-building corals. Obura (2012) demonstrated a decreasing coral species richness southward in the Mozambique Channel. A similar decreasing trend was observed in this study for the Iles Eparses. Similarly, a higher species richness is recorded for Tanzania and the Seychelles than for Mozambique and Madagascar, the exception being KZN with higher species richness right at the south-western end of the Channel (Table 2). These biogeographical trends must, however, be considered with caution. Although the checklist, presented in Appendix A.2 and summarized in Table 2, is a representative census of the published literature available for the Mozambique Channel region (including results from the present study), sampling and taxonomic efforts were not similar for all localities, and it is obvious that species lists for large countries such as Mozambique and Madagascar are incomplete. With respectively 2470 and 4828 km of coastline, the species richness of Madagascar (340 spp.) and

Mozambique (226 spp.) appears relatively under-represented when compared to regions with shorter coastlines, e.g. KZN (ca. 550 km, 504 spp.), Seychelles (491 km, 431 spp.), Tanzania (1424 km, 505 spp.) or even Mauritius (177 km, 435 spp. in Bolton et al., 2012). The situation is similar for the Comoro Islands (incl. Mayotte), for which only 59 species have been listed when the nearby and smaller Glorioso Archipelago has thus far 170 taxa recorded (coastline lengths are from http://world.bymap.org/ Coastlines.html; species richness figures are from Table 2). The current lack of knowledge probably accounts for the low similarity observed between floras of the three Iles Eparses and Madagascar, Mozambique and the Comoros despite their geographical proximity. The fact that Europa, Juan de Nova and Glorioso share more species with Tanzania and the Seychelles, is likely to be an artefact of the better documentation of marine floral diversity in these countries. Overall the floras of the three islands were mostly a subset of the regional diversity, representing 23.5% of the species richness of the Mozambique Channel, although they appeared individually quite contrasted. Differences in sampling effort may explain the decreasing species richness pattern observed between Glorioso, Juan de Nova and Europa, but other explanations may include variation in area and diversity of available habitat, isolation, and the age of the islands. In a biogeographical study of the marine flora of the Island of Rodrigues (Mauritius), which is similar in size and species richness to the Iles Eparses studied here, Schils et al. (2004) concluded that the relatively poor marine flora was most likely the result of habitat unavailability. Furthermore, the isolation and young age of Rodrigues might be additional barriers to the colonization of available habitats. In the present study, the lower species richness recorded at Europa (134 spp.), as compared to the two other islands (157 & 170 spp.), can likely be explained by the combination of (i) smaller lagoon and reef area (17.5 km2 at Europa vs. 206.69 km2 at Juan de Nova and 196.56 km2 at Glorioso), (ii) lower sampling effort (17 sites at Europa vs. 26 & 27 at Juan de Nova and Glorioso), and (iii) a more isolated geographic situation (300 km: shortest distance from Europa to any other land vs. 100 & 140 km for Juan de Nova and Glorioso). The age of Europa is unlikely to explain its lower species richness, as all three islands are of volcanic origin (Guennoc et al., 2011); Europa and Glorioso were formed about 100e200 Myrs ago while Juan de Nova may be younger (Battistini, 1996; Guillaume et al., 2013). However, the variation in sea level in the region during recent glaciation events (Camoin et al., 2004) may have had an influence on the present-day species diversity and richness. Besides these differences, and despite being sampled at the same time of the year, a very low number of species were common to the three islands (33 spp., about 11%). Relatively few species were shared between Europa and Juan de Nova (42 spp.) and Europa and Glorioso (54 spp.), whereas Juan de Nova and Glorioso appeared more similar (79 spp.). Questions therefore arise about which

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mechanism(s) may determine these differences, and whether species common to the region maintain connectivity with areas of the mainland, or whether the islands are rather isolated from the rest of the region. 4.3. Regional connectivity The opening of the Mozambique Channel dates back to the splitting of Madagascar from the African continent about 170 Ma. It is unclear when exactly the Iles Eparses were formed but they are at present located in the middle of a very turbulent Channel. The present-day surface circulation in the Mozambique Channel is characterized by a complex combination of cyclonic and anticyclonic mesoscale eddies fed by the North and the South Madagascar Equatorial Currents (NEMC and SEMC) (Hancke et al., 2014). A number of studies have proposed mesoscale eddies as potential vectors of connectivity between the east coast of Africa and Madagascar (Quartly and Srokosz, 2004; De Ruijter et al., 2004; Tew Kai and Marsac, 2010; Marsac et al., 2014). Although the propagation of mesoscale eddies is relatively slow, these hypotheses have been corroborated by Hancke et al. (2014) who showed that drifters (and therefore organisms) could use a faster route along the frontal zones between eddies. Hence, during experiments, drifters' minimum travel time was as little as 62 days from the northern to the southern end of the Mozambique Channel, 51 days from south to north, 22 days from west to east and 15 days from east to west (Hancke et al., 2014). Results also show that drifters departing from the central-east coast of Madagascar could reach southern Mozambique in as little as 41 days. These figures match floating and survival times of a number of seaweed species (van den Hoek, 1987; Thiel and Gutow, 2005a, 2005b), a notable example being Sargassum C. Agardh (Mattio et al., 2013; Yatsuya, 2008). Among the 82 drifter trajectories illustrated by Hancke et al. (2014), we estimate that three could have connected Europa to western Madagascar, three to southern Mozambique, one to Northern Mozambique and one to Juan de Nova, all in 15e50 days. Europa was also directly in the route of most drifters from centraleast Madagascar to southern Mozambique (see Hancke et al., 2014) supporting connections to both south-eastern Madagascar and southern Mozambique. Interestingly, at least one species present at Europa could illustrate this connection: Laurencia natalensis Kylin, so far only known from South Africa, was recently observed in southern Mozambique, Europa and south-east Madagascar (Appendix A.2; Francis, 2014). Hancke et al. (2014) also demonstrated a high level of retention in the Comoros basin where drifters had rather erratic and dense trajectories, suggesting important mixing and connectivity in the northern section of the Mozambique Channel. We believe that this circulation pattern could contribute significantly to similarities observed between Juan de Nova and Glorioso, and that high similarity can be expected with marine floras of northern Mozambique, the Comoros and north-west Madagascar. 5. Conclusion While molecular sequence data are useful or even essential for identifying some taxa, the recent use of such data has also profoundly altered our view of algal diversity. For most groups of algae gene sequences have unveiled a much greater species diversity than previously thought based solely on morphology (reviewed in Cianciola et al., 2010; De Clerck et al., 2013; Verbruggen, 2014). This surge of cryptic or pseudocryptic species, however, leads to the ironic situation that species identification becomes progressively less straightforward when using DNA markers. The problem manifests itself most prominently in floristic studies and biodiversity

inventories, such as the present paper. Genera that have been studied extensively using DNA markers are often rich in species, but these genera are the ones with the lowest numbers of clearly identified taxa. This paper represents the first published checklist for the Iles Eparses and, to date, the most comprehensive record of marine macrophyte species for islands in the Mozambique Channel. Due to the longitudinal arrangement of the islands between the northern and southern ends of the Mozambique Channel and their relatively central positions, Europa, Juan de Nova and Glorioso appear to represent data points of particular biogeographical interest and could be critical ‘stepping stones’ for connectivity in the Mozambique Channel region. However, a more comprehensive assessment of species diversity in the region is necessary for a better understanding of marine macrophyte biogeography in the Mozambique Channel. This should especially involve molecular identification techniques, and concentrate on the coasts of Mozambique and Madagascar as well as the Comoros (including Mayotte). Authors contribution M.Z. and L.M. contributed equally to the present study by both participating in all three field expeditions, and collecting and processing all samples. All authors participated in either one or the other identification workshop except C.G. who performed the statistical analyses. All authors participated in the writing of the manuscript, led by L.M. Acknowledgements The BIORECIE research programme was led by the Centre Na tional de la Recherche Scientifique, Institut d'Ecologie et Environnement (CNRS-INEE) with financial support from the Institut National des Sciences de l'Univers (INSU), the Institut de Recherche veloppement (IRD), the Agence des Aires Marines pour le De ge es (AAMP), the Fondation pour la Recherche sur la BioProte  (FRB), the Terres Australes et Antartiques françaises diversite (TAAF), and the Veolia Environment foundation. We would like to warmly thank Pascale Chabanet for leading the BIORECIE program and offering this unique opportunity to sample in the Iles Eparses. We are very grateful to the military personnel stationed on each of the islands for providing accommodation, food, and help during our stay. All crew of Antsiva, which was chartered for the three BIORECIE Expeditions greatly contributed to this study and we thank them warmly, especially Nicolas and Anne. Many thanks also to all the scientific crew who participated in part or all of the three cruises for their help and support throughout the project: J. Poupin, €t, L. Bigot, C. Bourmaud, C. Conand, P. Durville, M. S. Andrefoue Fournier, R. Fricke, N. Gravier-Bonnet, H. Magalon, T. Mulochau, L. Mattio, J-B. Nicet, C. Russo and S. Turay. We are in debt to C. Vieira, C. Francis, S.-M. Lin, S.-L. Liu, W. Prud’Homme van Reine, J. Roessger, L. Millet, F. Leliaert, L. Lagourgue, F. Mineur, V. Johnson, H. Verbruggen and L. Dijoux for their kind contributions towards the correct identification of our specimens. Finally, we would like to acknowledge the University of Cape veloppement in Town and the Institut de Recherche pour le De a for workshop space. G.W.M., J.J.B. and R.J.A. thank the Noume South African National Research Foundation (NRF) for research grants. RJA acknowledges the support of DAFF. We also acknowledge two reviewers and editors of the journal for their useful comments and suggestions on the manuscript.

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