Global checklist of species of Grania (Clitellata: Enchytraeidae) with remarks on their geographic distribution

. A checklist of all currently accepted species of Grania Southern, 1913 (Annelida, Clitellata, Enchytraeidae) is presented. The genus is widespread over the world and comprises 81 species described to date. Remarks on their geographical distribution, habitat, synonymies and museum catalogue numbers are provided. marine clitellates, geographic distribution, interstitial fauna.


Introduction
is a morphologically homogeneous and easily recognizable genus of marine Enchytraeidae Vejdovský, 1879 with a worldwide distribution. The worms are typically small, only a few mm long, with a fi liform, nematode-like body and a characteristic pattern of few, stout chaetae ( Fig.1). Most species live interstitially in intertidal or subtidal sands, but a few taxa are known from the deep sea.

Results
We report 81 currently accepted species of Grania, of which 49 are known from the Southern and 32 from the Northern Hemisphere. The only species found in both hemispheres (Atlantic Ocean) is the deep-sea Grania atlantica Coates & Erséus, 1985. Almost half of the known southern species (24) occur in Australia. On the other hand, 15 of the 32 species described from the Northern Hemisphere to date are European (Fig. 1).

Habitat
Intertidal, subtidal to 10 m, fi ne to coarse sand.

Paratype
The originally designated paratype AH 65 belongs to another species (see

Habitat
Intertidal, coarse sand and gravel.

Type locality
BERMUDA: Castle Island.

Habitat
Subtidal, 8-15 m, medium to coarse coral sand and gravel.

Habitat
Subtidal, 3-48 m, fi ne to coarse well-sorted sands and sand mixed with shell or shell gravel.

Distribution
West coast of Norway and Sweden, the Netherlands.

Habitat
Subtidal, 15-30 m, shell sand with gravel and pebbles or coarse sand with stones, pebbles and shells.

Habitat
Intertidal, subtidal to 7 m, fi ne to medium heterogeneous sand.

Type locality
RUSSIA: Sea of Okhotsk, Iturup Island.

Type locality
UNITED STATES: Santa Barbara, California.

Type locality
UNITED KINGDOM: Ascension Island, S Atlantic Ocean.

Habitat
Intertidal, among rocks and clumps of tubes of Sabellariidae.

Type locality
UNITED STATES: Georges Bank, SE of Massachusetts, NW Atlantic Ocean.

Type locality
UNITED STATES: off Maryland.

Habitat
Intertidal, subtidal to 65 m, medium to coarse sand.

Type locality
AUSTRALIA: Baker Bay, King George Sound, Western Australia.

Habitat
Subtidal, 4 m, fi ne sand with shells and seagrass.

Type locality
AUSTRALIA: Princess Royal Harbour, Albany area, Western Australia.

Habitat
Intertidal, subtidal to at least 6 m, fi ne to coarse sand and in sediments under boulders and in seagrass beds.

Type locality
AUSTRALIA: Princess Royal Harbour, Albany area, Western Australia.

Habitat
Intertidal, muddy coarse sand, gravel and mixed sand with pebbles and coral.

Type locality
AUSTRALIA: Princess Royal Harbour, Albany area, Western Australia.

Habitat
Intertidal, subtidal to 26 m, sand among boulders and pebbles, and with algal debris.

Type locality
AUSTRALIA: Middleton Beach, Albany area, Western Australia.

Habitat
Intertidal, sand among rocks in algal wash.

Type locality
AUSTRALIA: Baker Bay, King George Sound, Western Australia.

Type material
Holotype AUSTRALIA: Western Australia, Rottnest Island .

Type locality
AUSTRALIA: Rottnest Island, Western Australia.

Type material
Holotype AUSTRALIA: Western Australia, Rottnest Island .

Type locality
AUSTRALIA: Rottnest Island, Western Australia.

Type material
Holotype AUSTRALIA: Western Australia, Rottnest Island .

Type locality
AUSTRALIA: Rottnest Island, Western Australia.

Type material
Holotype AUSTRALIA: Western Australia, Rottnest Island .

Type locality
AUSTRALIA: Rottnest Island, Western Australia.

Type locality
ANTARCTICA: Ross Island.

Habitat
Subtidal, 38 m, greyish brown gravelly mud with sponge spicules and valves of Limatula.

Type locality
ANTARCTICA: Ross Island.

Type locality
ANTARCTICA: Ross Island.

Type locality
ANTARCTICA: Ross Island.

Type locality
ANTARCTICA: Ross Island.

Habitat
Subtidal, 35 m, fi ne sand with mica shale, shell debris and some pebbles.

Type locality
ANTARCTICA: Ross Island.

Type locality
AUSTRALIA: Darwin, Northern Territory.

Habitat
Intertidal, subtidal to 16 m, medium to coarse sand, clay or silty sediments.

Type locality
AUSTRALIA: Darwin, Northern Territory.

Type locality
AUSTRALIA: Darwin, Northern Territory.

Habitat
Intertidal crevices with sand gravel, pebbles and heterogeneous sediments.

Type locality
UNITED KINGDOM: South Georgia, SW Atlantic Ocean.

Type locality
UNITED KINGDOM: South Georgia, SW Atlantic Ocean.

Habitat
Intertidal, sediments trapped in dense turf of Corallina offi cinalis on horizontal or gently sloping rock.

Type locality
BERMUDA: Paget Island.

Habitat
Intertidal, subtidal to 17 m, medium to coarse sand with rocks.

Habitat
Intertidal pools with accumulation of sand and fi ne to medium-coarse calcareous sand.

Habitat
Intertidal, sand and gravel.

Habitat
Subtidal, 12-17 m, fi ne and muddy sands associated with beds of the seagrass Cymodocea nodosa.

Type locality
MOROCCO: off Casablanca.

Type locality
FRANCE: Gulf of Gascogne, lower continental slope.

Habitat
Deep sea, 2630-2885 m, most likely very fi ne sediments.

Habitat
Barely subtidal, 0.5 m, medium to coarse sand.

Distribution
Only known from the type locality.

Habitat
Intertidal, subtidal to 6 m, fi ne to coarse sand.

Habitat
Intertidal and barely subtidal, coarse sand and gravel.

Distribution
Only known from the type locality.

Type material
Holotype AUSTRALIA: Western Australia, New Island (WAM V 7315).

Type locality
AUSTRALIA: New Island, Western Australia.

Habitat
Intertidal, medium to coarse sand.

Type locality
AUSTRALIA: Lucky Bay, Western Australia.

Type locality
AUSTRALIA: Heron Island, Great Barrier Reef, Queensland, Australia.

Type locality
AUSTRALIA: Heron Island, Great Barrier Reef, Queensland, Australia.

Type locality
AUSTRALIA: Heron Island, Great Barrier Reef, Queensland, Australia.

Type locality
AUSTRALIA: Heron Island, Great Barrier Reef, Queensland, Australia.

Habitat
Intertidal, subtidal to 7 m, medium to coarse sand with some mud and lots of mollusc and barnacle shells.

Type locality
SOUTH AFRICA: Western Cape.

Habitat
Intertidal, coarse sand in rock crevice.

Type locality
SOUTH AFRICA: Western Cape.

Type locality
SOUTH AFRICA: Western Cape.

Type locality
SOUTH AFRICA: Western Cape.

Habitat
Intertidal, sand among rocks and heterogeneous sand with organic material.

Type locality
UNITED STATES: off North Carolina.

Type material
Holotype UNITED STATES: off North Carolina (USNM 1283174).

Type locality
UNITED STATES: off North Carolina.

Distribution
Only known from the type locality.

Discussion
Despite the many species of Grania described from the Australian continent and a few other southern regions of the globe (e.g., New Caledonia and Antarctica, see Fig. 2), taxa from the African and South American continents have been completely ignored until recently. This situation changed with the seven new species recently described from Brazil (1), Chile (2) and South Africa (4 spp.) (Prantoni et al. 2016).
The geographical distribution of the various species of Grania is strongly concordant with the phylogeny of the genus, as estimated by analyses of molecular data (De Wit et al. 2011;Prantoni et al. 2016). Most of the individual species appear to be endemic to rather small geographical areas, which suggests a limited capability of dispersion. However, as a whole, the genus is divided into at least three distinct evolutionary lineages, each with a broad, but geographically coherent distribution in the world; this is based on a sample of 28 genetically analyzed species (Prantoni et al. 2016). The fi rst lineage (green numbers on Fig. 2) comprises species from the Atlantic Ocean (including a sublineage of four species from South Africa). The second (blue numbers) are species from Australia and southern Asia (Hong Kong), and the third are species from the South Pacifi c and Atlantic regions (red numbers). An interesting aspect is the phylogenetic placement of G. americana in the North Atlantic and G. brasiliensis in the South Atlantic. These two species belong to an otherwise Pacifi c group (the third lineage), and it is suggested that they share a common ancestor that migrated from the Pacifi c region before the closing of the Isthmus of Panama 3 Ma (De Wit et al. 2011;Prantoni et al. 2016). However, as most Neotropical coasts remain unexplored, additional species of Grania from both sides of South America are needed to corroborate (or refute) this hypothesis.
In conclusion, more intense sampling efforts in many parts of the world are crucial to enable further studies of the evolutionary and biogeographical history of Grania. The 81 species described to date is a high number for a marine genus of Enchytraeidae, and yet, this number certainly does not represent the actual diversity of the genus Grania. Overall, our systematic knowledge of marine clitellates (oligochaetes and leeches) is poor, with perhaps only about 10% of the species diversity known (Appeltans et al. 2012). The lack of specialists around the world is evidently one of the reasons for this (Prantoni et al. 2014), but it is also a threat to any rapid improvement of the situation. As a partial solution, the combined efforts of taxonomists and ecologists may come as a fi rst and necessary step towards a better understanding of the group as well as of marine clitellate species diversity as a whole.