Additions to the South African sea anemone ( Cnidaria , Actiniaria ) fauna , with expanded distributional ranges for known species

The last monograph on South African sea anemones was published by Carlgren more than 75 years ago. Since that time, very little taxonomic research has been undertaken on this group and only seven additional species have been added to the regional fauna. In this study we document the history of taxonomic research and of species discovery for the South African anemone fauna, report on further additions to the fauna, and document expanded distributional ranges of known species. This study presents data from our own collections, as well as from the examination of historical data and museum collections, and from photographic records and specimens collected by SCUBA divers. Based on these data, two newly-discovered, but still un-described species, along with 12 new records, are added to the list of South African sea anemones. In addition, the ranges of 39 previously-known species are expanded. These new discoveries raise the total number of Actiniaria and Corallimorpharia species recognised from South African waters to 63.


Introduction
The first anemone record from South African waters was Actinia capensis in 1830, now accepted as Bunodosoma capense (Lesson, 1830).No further new discoveries that remain valid today were made until 1857, when Cystiactis reynaudi, now called Bunodactis reynaudi, was described from the Cape of Good Hope (Milne Edwards 1857).Verrill (1865Verrill ( , 1867Verrill ( , 1869) ) then described three new species, now called Haloclava capensis, Corynactis annulata and Anthothoe stimpsonii.This was followed by the description of Anthopleura michaelseni by Pax (1926) and by the addition of 10 species collected during the German deep-sea expedition on the steamer "Valdivia" two years later (Carlgren 1928a).In 1938, Carlgren made what has been the most significant contribution to South African Actiniarian systematics to date, by recording an additional 23 species from the region (Carlgren 1938) in his 'Monograph of South African Actiniaria and Corallimorpharia' and raising the total number of South African actiniaria up to 41 species.Following Carlgren's work, more than 40 years passed without any additional species being added to the anemone fauna, after which Dunn (1981) mentioned the presence of three tropical species, Entacmaea quadricolor, Heteractis magnifica and Stichodactyla mertensii in South Africa and England and Robson (1984) discovered Preactis millardae.This was followed by reports of two alien introductions in the region -Metridium senile from Cape Town Harbour, Table Bay (Griffiths et al. 1996) and Sagartia ornata from Saldanha Bay (Acuña et al. 2004).Subsequent to this, Schama et al. (2012) found that South African representatives of the species long known as 'Actinia equina' in fact represented an un-described, endemic species, which they named Actinia ebhayiensis.Finally, in the most recent addition to the fauna, Daly et al. (2012) described Edwardsia isimangaliso from Lake St Lucia.
Apart from these few taxonomic studies and a review of the species richness, endemicity and distribution patterns of the anemone fauna by Acuña and Griffiths (2004), no recent work has been undertaken on the South African sea anemones, resulting in an underestimation of both the richness of South African fauna and the distributional ranges of known species.In this study we contribute to the rectification of these shortcomings by collating an assortment of new data from museum collections, trawl surveys, SCUBA collected records, and our own field surveys to add both new anemone species to the South African fauna and to better document the true distributional ranges of existing species.

Material and methods
During three intensive sampling trips around South Africa, animals were gathered for examination from the east, south and west coasts.Areas mentioned in the text are displayed on a map in Figure 1.
Anemones were collected from the rocks using a specialised scraper tool, relaxed using 5 ml of menthol crystals placed into sea water, and fixed in formalin.After three days, the formalin was replaced with 70% ethanol.Two collection methods were used during these surveys: collection off rocks exposed during spring low tide and collection from up to 30 m depth by SCUBA divers.As collection permits for Sodwana Bay and Rocktail Bay were not granted for this study, due to the value of these anemones to the SCUBA diving ecotourism industry, only photographic records were obtained in these areas.Following identification of wet material, all specimens were deposited in the Iziko South African Museum (SAM) marine invertebrate collection, along with digital copies of photographs and an Excel database containing details of all records.Synonymy lists were adapted from Hexacorallians of the World (Fautin 2013).
Additional datasets from previous rocky shore intertidal surveys around South Africa were generously provided by Dr Kerry Sink and Dr Angela Mead, and photographic records provided by recreational SCUBA divers were also included where the species could be identified with confidence.Additional specimens examined for this study included previously unexamined specimens from the Iziko South African Museum (SAM) collection, which included specimens collected by the University of Cape Town (UCT) Ecological Survey and specimens collected by the Department of Agriculture, Forestry and Fisheries (DAFF) during routine deep-sea trawl surveys.
Attached to the locality data are depth records, enabling a depth range to be determined for each species.For the purposes of this study, the west coast was defined as stretching from the Namibian border to Cape Point, the south coast as stretching eastwards from Cape Point to the Mbashe River in the Transkei, and the east coast as stretching from the Mbashe River northwards to the Mozambique border.

History of discovery
Figure 2 shows a timeline of the numbers of Actiniarian and Corallimorpharian species recorded from South Africa over the last two centuries.The enormous contributions made by Carlgren (1928aCarlgren ( , 1938) ) are particularly striking, as is the very low level of taxonomic activity over the subsequent decades until present.Fourteen species new to South Africa were recorded during this study, including two new species currently undergoing description, making this the most significant contribution in terms of expansion of the fauna list since the monograph of Carlgren (1938).Following this study, the total number of Actiniaria and Corallimorpharia species recognised from South African waters is raised to 63.

New additions to the fauna
The samples and data sources examined resulted in the addition of 14 anemone species to the South African fauna.These comprise two species new to science, both of which are currently being formally described elsewhere, plus 12 species new to the region.The following account summarises the previously known range of each of these species, details where South African specimens were found, mentions similar species known from South Africa, and lists museum specimens and selected photographs of each of the new species recorded.
Table 1 summarises the specimen and photographic data for each of the new records.Five of these new records are based on photographic evidence, while specimens exist for the remaining seven.

Species new to science Family Halcampidae Andres, 1883 Genus Halianthella Kwietniewski, 1896
Halianthella sp.n.Fig. 3A This very tiny species was discovered by Helen and Guido Zsilavecz while diving at 15 m in False Bay, near Cape Point.Specimens were sent to Dr Estefanía Rodríguez, assistant curator of the American Museum of Natural History, who is in the process of describing this material as a new species in the genus Halianthella.This species is thus referred to here as Halianthella sp.n., and it is known to SCUBA divers as the 'clown anemone'.The second new species, known to divers as the 'dwarf spotted anemone', was first collected by Prof. Charles Griffiths from Oudekraal.This species is referred to here as Anthostella sp.n. as the formal publication of the description by Dr Estefanía Rodríguez and Dr Megan Laird is still pending.

Species newly reported from South Africa
Family Actinernus plebeius McMurrich, 1893: 165-167, pl. 24, figs 42-45;Carlgren 1896: 174;Gravier 1918: 6-7;1922: 31-32 Actinoscyphia plebeian: Fautin 1984: 37-40;Rodríguez 2012: 215 This species is previously known from Antarctica, Chile and the South Georgia Islands off Argentina.The addition of this species to the South African fauna is based on multiple trawl records from both the west and south coasts of South Africa collected by the Department of Agriculture, Forestry and Fisheries (DAFF) during annual trawl surveys.According to available records, it was first found in 2007 on the Agulhas Bank, but those specimens remained unidentified until this study.Three specimens are lodged in the Iziko South African Museum (SAM): H5181, H5179 and H5178 (Table 1) and additional records are based on trawl data with no supporting specimens.The distribution range of this species extends from Kleinzee on the west coast to the Agulhas Bank on the south coast, between 128-866 m depth.Actinoscyphia plebeia is distinguishable from Actinostola capensis, another deep-sea species found in the same area off the coast of South Africa, by the maroon coloration of its tentacles and oral disc, its smooth column and its slimy texture.

Family Haloclavidae Verrill, 1899 Genus Peachia Gosse, 1855
Peachia parasitica (Agassiz, 1859) Fig. 4B Bicidium parasiticum Agassiz, 1859: 23-24 Peachia parasitica: Verrill 1866: 338-339, 343;McDermott et al. 1982: 319-321 Previously known from east and west coasts of North America, as well as from the east coast of Greenland.The addition of this species to the South African fauna is based on a single specimen collected by Dr. Deborah Robertson-Andersson in 2011.The anemone was collected from Table Bay during a boat-based expedition targeting the collection of jellyfish.The juvenile was found attached to the underside of the medusa of the jellyfish Chrysaora fulgida.This specimen is lodged in SAM with catalogue number H5202 (Table 1).Peachia parasitica is distinguishable from Peachia sp.(below) by the unmarked tentacles and oral disc of the former, as well as the tendency of juveniles to live as parasites.
Peachia sp.Fig. 4C Due to a lack of well-preserved samples, it was not possible to determine the specific name of this anemone, thus the previous range is unknown.The addition of this species to the South African fauna is based on a single specimen found in 1 m of water and collected from Langebaan Lagoon in 2002.Two additional photographic records of this species exist, both from Port Elizabeth on the south coast, between 8-18 m depth.The specimen is lodged in SAM with catalogue number H5385 (Table 1).Peachia sp. is distinguishable from Peachia parasitica by the unmistakable chevron patterns on the tentacles.

Family Actiniidae Rafinesque 1815 Genus Pseudactinia Carlgren, 1928b
Pseudactinia sp.Fig. 4D As it was not possible to determine the specific name of this anemone, the previous range is unknown.The addition of this species to the South African anemone fauna is based on two specimens collected from Algoa Bay in 2008, as well as 34 photographic records from the south coast.The distributional range of this species is recorded from False Bay to Aliwal Shoal from 1-29 m depth.The two specimens are lodged in SAM: H5588 and H5599 (Table 1) and additional records are based on photographic records collected by recreational SCUBA divers.Photographic records are not listed in Table 1 and are obtainable from SAM. Pseudactinia sp. is large and has a very wide oral disc, like that of P. flagellifera, but has only one row of vesicles, while P. flagellifera has up to five.Pseudactinia varia is much smaller than Pseudactinia sp., but also has one row of vesicles.Pseudactinia sp. is unique in that the column is often mottled and the oral disc is striped.The distinction between species is not purely morphological, but is also based on molecular studies (Heestand 2009).
Megalactis griffithsi was first recorded in 2003 (Table 1) and is know from depths of 18-20 m.The original photograph remained unidentified until this species was again encountered during a research dive that formed part of this study in 2008.
Although the specimen was not collected, it was possible to observe the behaviour of the anemone, and based on this, as well as the external morphology visible in photographs, the species name was determined.Megalactis griffithsi is distinguishable from Actinodendron hansingorum and other species of the genus by the alternating dark and light areas between each segment of the oral disc.The number of secondary branches on the tentacles also does not exceed 35 in number (Ardelean and Fautin 2004).

Family Aliciidae Duerden, 1895 Genus Alicia Johnson, 1861
Alicia sansibarensis Carlgren, 1900 Fig. 4F Alicia sansibarensis Carlgren, 1900: 28-30;Parulekar 1990: 219-220, 223, 225;Pax 1909: 402;Stephenson 1922: 280;Carlgren 1927b: 444;1949: 43 This species was previously considered endemic to Zanzibar.The addition of this species to the South African fauna is based on one specimen from Sodwana Bay collected from 105 m depth in 2004.This specimen remained unidentified until now due to a lack of taxonomic expertise.The anemone is lodged in SAM with catalogue number H5158 (Table 1).Alicia sansibarensis is distinguishable from Triactis producta, the only other species of the family Aliciidae found in South Africa, by the division of the column of A. sansibarensis into a scapus and a capitulum.The tentacles of A. sansibarensis are very long and snake-like, while those of T. producta are short.

Heteractis malu (Haddon & Shackleton, 1893)
Fig. 5D Discosoma Malu Haddon & Shackleton, 1893: 117, 120 Heteractis malu Dunn, 1981: 35, 40, 47, 57, 66-71, 104, 107-108 Radianthus malu England, 1988: 53 This species is previously known from across most of the Indo-Pacific.The addition of Heteractis malu to the South African fauna is based on two photographic records from Sodwana Bay from 15-20 m, with the first taken by a SCUBA diver in 2004 (Table 1).The species was encountered again during a field survey for this study in 2008.Although the anemone was not collected, it was possible to conclusively determine the species based on external morphology visible in photographs.They show adhesive verrucae on the column, as well as short, sparse tentacles (Fautin et al. 2008).

Genus Stichodactyla Brandt, 1835
Stichodactyla haddoni (Saville-Kent, 1893) Fig. 5E Discosoma Haddoni Saville-Kent, 1893: 32-33. Carlgren 1896: 174 Stichodactyla haddoni Dunn, 1981: 82-91. Fautin and Allen 1992: 40-41. Fautin et al. 2009: 133 The range of this species extends across most of the Indo-Pacific.The addition of Stichodactyla haddoni to the South African fauna is based on three photographic records from Sodwana Bay in 14-20 m of water.The anemone was first recorded by a SCUBA diver in 2004, with two additional photographs taken in 2005 (Table 1).No South African specimens of this anemone are housed in SAM; however, a specimen from just north of the Mozambique border is in the museum collection.As this is a large anemone, it was possible to determine the species based on external morphology visible in photographs.Stichodactyla haddoni is usually easily distinguishable from S. mertensii, as S. haddoni is usually found in sand, has a weakly adherent pedal disc, has extremely sticky tentacles, has a column that is unable to contract completely, and has a maximum oral disc diameter of 500 mm.In contrast, S. mertensii is found attached to coral reef, has an extremely adhesive pedal disc, has non-adherent tentacles, is able to slowly contract into crevices (Fautin and Allen 1997) and has a maximum oral disc diameter of 1500 mm.

Range expansion
Since the work of Carlgren (1938) and the distributional review by Acuña and Griffiths ( 2004), a large amount of distributional data for anemones has been collected.These data have been stored in museums and on online databases such as 'Hexacorallians of the world' (Fautin 2013), but these ranges have never before been collated and published.
The range expansion of Metridium senile is the most notable, as this is one of two alien anemone species known in South Africa.This species was first recorded in South Africa from the Table Bay Harbour (Griffiths et al. 1996) in September 1995, when a well-established colony was discovered.Anemones were attached to artificial substrata, such as car tyres, at a depth of 10-16 m, and it is thought that the species was introduced to South Africa via shipping from Europe (Griffiths et al. 1996).However, in February 2006, another population of M. senile was discovered at 115 m on the PetroSA pipeline on the Agulhas Bank (35°13'59.08"S,21°29'53.44"E)by Dr Lara Atkinson.Individuals were morphologically identical to those of the Table Bay population and it was interesting to note that both populations were established on artificial structures.The size of each of these alien populations should be monitored annually to ensure that their range does not expand.
Other species for which range expansions have been detected since the work of Carlgren (1938) and Acuña and Griffiths (2004) are listed in Table 2.The distribution ranges of eight species were extended to the west, 18 species to the east, and 13 species to both the west and the east (Table 2).The fact that the ranges of so many species have been expanded, suggests that sea anemones around the South African coastline have been severely under-sampled in the past.

Discussion and conclusions
Since the writings of Carlgren (1927aCarlgren ( , 1928aCarlgren ( , 1938Carlgren ( , 1940aCarlgren ( , 1949)), very little South African work has been done on the taxonomy of this group.The most recent species list available is that compiled by Acuña and Griffiths (2004), who reported 49 species of sea anemones from South Africa.Following extensive fieldwork and examination of unidentified anemones in the Iziko South African Museum (SAM) during the course of this study, the number of sea anemone species know from South Africa is hereby increased to 63.This number is high in comparison to the 30 species reported from the Faroe Islands (Fautin et al. 2005) and the 26 species from Galicia in north-western Spain (den Hartog and Ates 2011), but is on a par with the 63 species recorded from Chile (Häussermann 2006).The South African sea anemone fauna makes up over 5% of the total anemone species worldwide when compared to the species list published by Daly et al. (2007).An increase of 14 species in one country over a relatively short study suggests that many more anemone species are still to be found in South Africa.The ranges of 79% of the anemone species reported by Acuña and Griffiths (2004) were also expanded by this study.Gaps in sample coverage remain particularly obvious in deep-sea areas, particularly the bathyal (500-3500 m) and the abyssal (3500-5000 m), the latter being essentially completely unexplored.Geographically, the west and east coasts need to be more thoroughly sampled, while estuarine habitats also need to be made a priority.
Eight of the 14 species added to the fauna were found on the east coast, with seven discovered by SCUBA divers and one collected in a trawl.Two of the new additions were found on the west coast, one a shallow water species found burrowing in sand and the other a pelagic species found on the medusa of a jellyfish.Two of the new records were found on the south coast by SCUBA divers, and a further two species were found to inhabit areas extending from the west to the south coast, with one found by SCUBA divers and the other retrieved by a deep-sea trawl.All of the east coast records are tropical forms previously well known from the Indo-Pacific.The use of SCUBA divers as a collection method for sea anemones has resulted in the addition of 10 of the 14 new records.This method was not available to Carlgren, which probably explains why these species were missed by him.As they occur at depths of 2 m and deeper, they are beyond the reach of rocky shore researchers, while at the same time being too shallow, or occurring in reef Table 2. Previous distribution and depth ranges and updated distribution and depth ranges for each anemone species that experienced an alteration in range.References for previous records are listed.Species range expansions were classified as being to the west (W), the east (E) or to both the west and east (W&E).A dash (-) indicates species that were found to have increased depth ranges.See Figure 1 for site locations.

Updated records
Exp.

Urticinopsis crassa
Cape Point 566-1024 Hondeklip Bay to Agulhas Bank 143-1024 W&E Carlgren 1938 habitats that could not be sampled using ship-borne equipment such as grabs, dredges and trawl nets.This emphasises the importance of recreational SCUBA divers in the discovery of new species within this and other groups that are abundant on shallow rocky reefs.

Figure 1 .
Figure 1.Map of South Africa showing places mentioned in the text: 1 St Helena Bay 2 Cape Columbine 3 Saldanha Bay 4 Langebaan Lagoon 5 Table Bay 6 Sea Point 7 Oudekraal 8 Kommetjie 9 Cape of Good Hope 10 False Bay 11 Cape Hangklip, and 12 Bhanga Nek (Mozambique border).

Figure 2 .
Figure 2. The number of species recorded from South Africa between 1830 and 2015.

Figure 3 .
Figure 3.The two new species of sea anemone reported in this study: A Halianthella sp.n. (3 mm) and B Anthostella sp.n. (10 mm).Photographs taken by Guido Zsilavecz (A) and Megan Laird (B).

Table 1 .
Selected specimen and photographic records of the 12 species recorded in South Africa for the first time.Records based on photographs are only listed if no specimens are available.'Cat #' refers to the category number of the specimen lodged in SAM, 'Station #' refers to the site where the specimens were collected and 'Photograph #' refers to the file name of the photograph lodged at SAM.