Sphaeroma terebrans

Invasion History

First Non-native North American Tidal Record: 1881
First Non-native West Coast Tidal Record:
First Non-native East/Gulf Coast Tidal Record: 1881

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General Invasion History:

Sphaeroma terebrans was described by Bate in 1866, from Brazil (Richardson 1905). It is now widely distributed in tropical-subtropical regions, including the Indo-Pacific from Taiwan to Australia; South Africa and along the West coast of Africa; and the Atlantic coast of South and North America, where it has been collected as far north as Virginia (Schultz 1969; Harrison and Holdich 1989; Kensley and Schotte 1989; Davidson et al. 2014). It was originally described from Brazil in 1866, but its close affinity to Indian Ocean species, its absence of planktonic larvae, and the well documented recent introductions of related Indo-Pacific species (S. annandalei, S. walkeri, S. quoianum) indicate that S. terebrans was probably transported to the Atlantic on the hulls of wooden ships before 1850 (Carlton and Ruckelshaus 1997). Carlton and Ruckelshaus (1997) predict that no evidence of S. terebrans boring into mangrove roots will be found in sediments predating European colonization. Genetic analysis indicates that 'S. terebrans' is a complex of at least four species (Baratti et al. 2005; Baratti et al. 2011). Two of these clades (A and B) coexist on the Indian Ocean coast of Africa. Populations in Florida and Brazil were assigned to Clade C, closely related to Clade B. Baratti et al. (2005 and 2011) attribute the global distribution of these forms, with subsequent speciation to natural dispersal, by rafting. However, they have examined only a small portion of the range of S. terebrans and cannot exclude the possibility that species C exists elsewhere in the Indo-Pacific.

North American Invasion History:

Invasion History on the East Coast:

The first North American record of Sphaeroma terebrans (as S. destructor), that we know of, was from Crescent City, Florida, near the headwaters of the St. Johns River in 1881 (US National Museum of Natural History 2009). Another collection was made in the Colleton River, South Carolina in 1891 (US National Museum of Natural History 2009). This isopod was formally described as S. destructor from the pilings of a bridge in freshwaters of the St. Johns River, Palatka, Florida (Richardson 1897). It was collected near Lake Pontchartrain, Louisiana, in 1906 (US National Museum of Natural History 2009). The regular range of this isopod appears to be from South Carolina to Texas, and southward to Cuba, Belize, and Brazil (Richardson 1897; Richardson 1905; Wallour 1960; Menzies and Frankenberg 1966; Miller 1968; Kensley and Schotte 1989). In Florida, S. terebrans is distributed around much of the peninsula, but was absent from about half of the 51 sites surveyed, including the Keys and the southernmost tip (Conover and Reid 1975). Sphaeroma terebrans was recorded only once from Chesapeake Bay, from the hull of a boat in Urbanna, Virginia, near the mouth of the Rappahannock River (Miller 1968; Van Engel 1972; United States National Museum of Natural History collections). It was considered a 'stray, unlikely to become established' (Van Engel 1972).

Invasion History Elsewhere in the World:

Outside the continental United States, Sphaeroma terebrans is found in Mexico (Montalvo-Urgel et al. 2010); Cuba (1994, USNM 280038, US National Museum of Natural History 2009); Belize (1980, USNM 205619, US National Museum of Natural History; Davidson et al. 2016); Costa Rica (Villalobos et al. 1985); Colon, Panama (Caribbean, Davidson et al. 2016); and Venezuela (1987, USNM 234047, US National Museum of Natural History 2009). We follow Carlton and Ruckelshaus (1997) in considering S. terebrans a likely very early introduction to the tropical Western Atlantic. However, paleontological studies of mangrove communities, and genetic studies are desirable to clarify the history and origin of this isopod.

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Description

Sphaeroma terebrans has a compact, convex, elliptical body, which is about twice as long as it is wide. The posterior-dorsal surface of the body, and particularly the pleoteloson, is covered with tubercles. The head is approximately semicircular, with prominent eyes, composed of many ocelli. Antenna 1 has a flagellum of 11 segments and extends to the posterior edge of Peraeonite 1. Antenna 2's flagellum has 16 segments and reaches the posterior edge of Peraeonite 2. The peraeonites are roughly equal in width. Peraeonites 2-4 each bear a broad transverse ridge, while Peraeonites 4, 6, and 7 each bear four large tubercles. The pleotelson is roughly triangular and covered with tubercles. Many of the tubercles bear clusters of hairs. Pereiopods 1-3 bear dense plumose setae on the upper (anterior) surface of segments 3-4, an adaptation for filter-feeding. The outer edges of the exopods of the uropods each bear five prominent teeth. Adults are 8-12 mm long and are brown-to-reddish brown. They frequently roll into balls when disturbed. This description is based on: Richardson 1905, Van Name 1936, Schultz 1969, Harrison and Holdich 1984, Kensley and Schotte 1989, Theil 1999, and Hossain and Bamber 2013.

Isopods identified as S. terebrans are widely distributed in subtropical and tropical waters, and show substantial morphological and genetic variation. Specimens from the Western Atlantic were described as S. destructor (Richardson 1897, cited by Richardson 1905). Sphaeroma terebrans is usually treated as synonymous with S. destructor (Van Name 1936; Miller 1968; Harrison and Holdich 1984), but sometimes with uncertainty (Kensley and Schotte 1989). Genetic studies (Baratti et al. 2005; Baratti et al. 2011) indicate a high degree of genetic diversity, suggesting that 'S. terebrans' is a complex of several species. However, some of the sharpest differences are between Clades A and B, both on the coast of East Africa, while the Western Atlantic clade (Florida-Brazil) is closely related to Clade B. The number of sites sampled was relatively small, compared to the large range of the species. Therefore, further genetic studies are needed to describe the genetic diversity and biogeographic history of the species.

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Taxonomy

Ecology

General:

Sphaeroma terebrans has separate sexes, with internal fertilization, brooded young and direct development. Females carry 10-80 embryos, with broods tending to increase with body size from 7.5 to 12 mm body length. Sphaeroma terebrans exhibits extended parental care, in which early juveniles remain in the parental burrow until they develop the ability to burrow and filter-feed. Females usually host 5-20 juveniles in their burrows (extremes 1-58). Juveniles in burrows were usually 2-3 mm in size. Males do not remain in the females' burrows after copulation. In the Indian River Lagoon, Florida, juveniles were scarce in January through March, and most abundant and June (Thiel 1999).

Sphaeroma terebrans occurs in warm-temperate to tropical climates, and tidal fresh to euhaline waters (Richardson 1905; Van Name 1936; Kensley and Schotte 1989; Wilkinson 2002). It bores into mangrove roots, Bald Cypress roots, and roots of fresh-brackish marsh plants (at least six different species). Borers were found in intertidal and shallow subtidal pilings, rotten wood, and Styrofoam floats (Richardson 1905; Rehm and Humm 1973; Estevez 1994; Wilkinson 2002). In more saline waters in Florida and the Caribbean, the most common substrates are the prop roots of Red Mangrove (Rhizophora mangle) (Rehm and Humm 1973; Brooks 2004; Brooks and Bell 2005; Davidson et al. 2016). This isopod is also occasionally found in branches and roots of White (Laguncularia racemosa) and Black Mangroves (Avicennia nitida). Burrow length is usually correlated with isopod size and the largest burrows reported (9-12 mm) were made by isopods 7-9 mm long. Animals from brackish-water areas had normal burrows at low (3 PSU) and medium salinities, but greatly reduced burrowing at high (30 PSU) salinity. However, effects of long-term acclimation and genetic variation were not examined (John 1970). There has been some debate as to whether S. terebrans obtains any nutrition from the wood or plant material that it consumes. A recent morphological study concluded that S. terebrans primary feeds by suspension-feeding on detritus and phytoplankton, and uses the wood primarily as shelter (Si et al. 2002). This isopod's burrow may limit predation.

A commensal isopod, Iais floridana has been found living in the burrows of S. terebrans in the Indian River Lagoon, Florida. This isopod has not been found elsewhere, but it closely resembles the Indo-Pacific I. singaporensis (Kensley and Schotte 1999). We consider I. floridana a likely introduction. Its effects on S. terebrans have not been studied, but a similar commensal, I. californica had no effects on the growth and survival of its host, S. quoianum, introduced to the West Coast (Rotramel 1975). Another, more unusual interaction with an isopod species, occurs in Florida, when juveniles of S. quadridentata invade the burrows of female S. terebrans, apparently benefiting from the other species parental care. The presence of the invading juveniles may decrease the duration of parental care for the females' own juveniles (Thiel 2000).

Food:

Phytoplankton, Detritus, Wood?

Trophic Status:

Suspension Feeder

SusFed

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Habitats

General Habitat	Nontidal Freshwater	None
General Habitat	Tidal Fresh Marsh	None
General Habitat	Marinas & Docks	None
General Habitat	Coarse Woody Debris	None
General Habitat	Mangroves	None
General Habitat	Vessel Hull	None
Salinity Range	Limnetic	0-0.5 PSU
Salinity Range	Oligohaline	0.5-5 PSU
Salinity Range	Mesohaline	5-18 PSU
Salinity Range	Polyhaline	18-30 PSU
Salinity Range	Euhaline	30-40 PSU
Tidal Range	Subtidal	None
Tidal Range	Low Intertidal	None
Vertical Habitat	Epibenthic	None

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Tolerances and Life History Parameters

Minimum Temperature (ºC)	8	Field, Bonnet-Carre Spillway, Lake Pontchartrain LA (Wilkinson 2002)
Maximum Temperature (ºC)	34	Fort Pierce, Florida (Field, Thiel 1999)
Minimum Salinity (‰)	0	Field (Richardson 1897).
Maximum Salinity (‰)	39	Field data, Florida Bay (Brooks 2004)
Minimum Length (mm)	9.5	Van Name 1936
Maximum Length (mm)	11.5	Female (Van Name 1936; Kensley and Schotte 1989)
Broad Temperature Range	None	Warm temperate-tropical
Broad Salinity Range	None	Fresh-Euhaline

General Impacts

In Florida and other tropical regions, Sphaeroma terebrans plays an important role by recycling dead wood (Becker 1971) and regulating the growth of mangroves (Rehm and Humm 1973; Ribi 1982; Simberloff et al. 1978; Perry and Brusca 1989; Davidson et al. 2014), and also as a borer in tidal marsh vegetation (Estevez 1994). This isopod is also an economically important borer on submerged wooden structures, such as pilings (Atwood 1920; Becker 1971; Wilkinson et al. 2002). It has been found burrowing in Styrofoam floats, and damaging them in Lake Pontchartrain, Louisiana; Colon, Panama; the Philippines and Taiwan (Wilkinson et al. 2002; Davidson 2012).

Herbivory- S. terebrans does not consume wood directly, but uses it for shelter, tunneling into it and filter-feeding, and also probably feeding on bacteria, fungi etc. growing on the tunnel walls (Becker 1971; Estevez 1945). However, a cellulase has been reported from some wood-boring Sphaeroma spp, so direct consumption of wood cannot be ruled out (Becker 1971). A more recent morphological study concludes that S. terebrans primary mode of feeding is suspension-feeding on detritus and phytoplankton (Si et al. 2002). Sphaeroma terebrans burrows into the aerial roots of Rhizophora mangle (Red Mangrove) (Humm and Rehm 1973), hollowing them out, and also into the rhizomes of Juncus roemerianus (Black Needle Rush) plants in tidal marshes (Estevez 1994).

Habitat Change – S. terebrans clearly has an important role in the dynamics of Rhizophora mangle (Red Mangrove) communities, but the precise nature of its effects on mangrove communities has been subject of study and debate. Initially, it was regarded as a destroyer of mangroves (Humm and Rehm 1973), but S. terebrans were also found to increase the frequency of root branching (Simberloff et al. 1978) and to differentially infest roots farther from established roots, resulting in increased density of roots near the stand (Ribi 1982). However, Perry and Brusca (1989), working with the similar Pacific S. peruvianum, found that the mangrove's responses to herbivory did not offset the loss of productivity due to Sphaeroma's burrowing. Sphaeroma terebrans effects on marsh vegetation could also encourage marsh erosion (Estevez 1994).

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Regional Impacts

CAR-I	Northern Yucatan, Gulf of Mexico, Florida Straits, to Middle Eastern Florida		Ecological Impact	Habitat Change
Extensive damage to roots of Red mangrove (Rhizophora mangle) was found with 70-100% of mangrove roots infested, and 20-100% of roots severed (Rehm and Humm 1973; Conover and Reid 1975). Extensive burrowing was also found in tidal brackish and fresh marshes of tributaries of Tampa Bay and Charlotte Harbor, in peat and roots of Juncus plants. Burrows were especially common on the scarps of receding marshes, and could be accelerating marsh retreat (Estevez 1994). In experiments, R. mangle responds to boring activity by increasing the number of root endings in unparasitized roots, mostly those already buried in soil. Sphaeroma terebrans' boring activity could actually increase the stability of shorelines (Simberloff et al. 1978; Ribi 1982). However, in caging experiments in Rookery Bay (Bear Creek and Environmental Learning Center) and Braden River, exclusion of S. terebrans resulted in much more extensive growth and complexity of mangrove roots. Boring by S. terebrans may limit the seaward growth of the mangrove community (Davidson et al. 2016). Boring by S. terebrans in plastic foam floats contributes to pollution by plastic particles, with adverse consequences to marine foodwebs (Davidson 2012). In Lake Pontchartrain, Louisiana, S. terebrans extensively bored into Bald Cypress (Taxodium distichum) stumps, honeycombing them, and contributing to their decay and shoreline erosion (Wilkinson 2002).
CAR-I	Northern Yucatan, Gulf of Mexico, Florida Straits, to Middle Eastern Florida		Economic Impact	Shipping/Boating
Sphaeroma terebrans has caused damage to docks, pilings, and boat hulls (Atwood 1932). Damage to plastic floats was extensive in southwest Florida and in Lake Pontchartrain LA (Davidson 2012).
G070	Tampa Bay		Ecological Impact	Habitat Change
Extensive damage to roots of Red mangrove (Rhizophora mangle) was found with 70-80% of mangrove roots infested, and 20-40% of roots severed (Conover and Reid 1975). In caging experiments in Rookery Bay (Bear Creek and Environmental Learning Center) and Braden River, exclusion of S. terebrans resulted in much more extensive growth and complexity of mangrove roots (Davidson et al. 2016). Extensive burrowing was also found in tidal brackish and fresh marshes, in peat and roots of Juncus plants. Burrows were especially common on the scarps of receding marshes, and could be accelerating marsh retreat (Estevez 1994). Boring by S. terebrans in plastic foam floats contribute to pollution by plastic particles, with adverse consequences to marine foodwebs (Davidson 2012).
G074	_CDA_G074 (Crystal-Pithlachascotee)		Ecological Impact	Habitat Change
Extensive damage to roots of Red Mangrove (Rhizophora mangle) was found with 90% of mangrove roots infested, and 60% of roots severed (Conover and Reid 1975).
G050	Charlotte Harbor		Ecological Impact	Habitat Change
Extensive damage to roots of Red Mangrove (Rhizophora mangle) was found with 90-100% of mangrove roots infested, and 50-80% of roots severed (Conover and Reid 1975).
G045	_CDA_G045 (Big Cypress Swamp)		Ecological Impact	Habitat Change
Extensive damage to roots of Red Mangrove (Rhizophora mangle) was found with 80-100% of mangrove roots infested, and 20-80% of roots severed (Conover and Reid 1975).
G030	North Ten Thousand Islands		Ecological Impact	Habitat Change
Extensive damage to roots of Red Mangrove (Rhizophora mangle) was found with 100% of mangrove roots infested, and 80-100% of roots severed (Rehm and Humm 1973; Conover and Reid 1975). In caging experiments in Rookery Bay (Environmental Learning Center, Bear Creek), exclusion of S. terebrans resulted in much more extensive growth and complexity of mangrove roots (Davidson et al. 2016).
G020	South Ten Thousand Islands		Ecological Impact	Habitat Change
Extensive damage to roots of Red Mangrove (Rhizophora mangle) was found with 100% of mangrove roots infested, and 80-100% of roots severed (Conover and Reid 1975).
G010	Florida Bay		Ecological Impact	Habitat Change
Extensive damage to roots of Red Mangrove (Rhizophora mangle) was found with 70% of mangrove roots infested, and 20% of roots severed (Conover and Reid 1975).
S200	Biscayne Bay		Ecological Impact	Habitat Change
Extensive damage to roots of Red Mangrove (Rhizophora mangle) was found with 80-100% of mangrove roots infested, and 60-100% of roots severed (Conover and Reid 1975). However, in experiments, R. mangle responds to boring activity by increasing the number of root endings in unparasitized roots, mostly those already buried in soil. Sphaeroma's boring activity could actually increase the stability of shorelines Simberloff et al. 1978; Ribi 1982).
S196	_CDA_S196 (Cape Canaveral)		Ecological Impact	Habitat Change
Extensive damage to roots of Red Mangrove (Rhizophora mangle) was found with 100% of mangrove roots infested, and 90% of roots severed (Conover and Reid 1975).
S190	Indian River		Ecological Impact	Habitat Change
Extensive damage to roots of Red Mangrove (Rhizophora mangle) was found with 80-100% of mangrove roots infested, and 30-60% of roots severed (Conover and Reid 1975).
CAR-III	None		Ecological Impact	Habitat Change
In field observations in Costa Rica, Red Mangrove (Rhizophora mangle responds to boring activity by increasing the number of root endings in unparasitized roots, mostly those already buried in soil. Sphaeroma's boring activity could actually increase the stability of shorelines (Simberloff et al. 1978; Ribi 1982; Villalobos et al. 1985). However, in caging experiments in Galeta and Boca del Drago, Panama, exclusion of S. terebrans resulted in much more extensive growth and complexity of mangrove roots (Davidson et al. 2016).
G070	Tampa Bay		Economic Impact	Shipping/Boating
Sphaeroma terebrans has caused damage to docks, pilings, and boat hulls (Atwood 1920). Damage to plastic floats was extensive in southwest Florida and in Lake Pontchartrain LA (Davidson 2012).
G170	West Mississippi Sound		Ecological Impact	Habitat Change
In Lake Pontchartrain, Louisiana, S. terebrans extensively bored into Bald Cypress (Taxodium distichum) stumps, honeycombing them, and contributing to their decay and shoreline erosion (Wilkinson 2002; Davidson 2012).
G170	West Mississippi Sound		Economic Impact	Shipping/Boating
Sphaeroma terebrans has caused damage to docks, pilings, and boat hulls (Atwood 1920). Damage to plastic floats was extensive in southwest Florida and in Lake Pontchartrain LA (Davidson 2012).
CAR-III	None		Economic Impact	Shipping/Boating
Damage to plastic floats was extensive in Colon, Panama (Davidson 2012). Boring by S. terebrans in plastic foam floats contirbute to pollution by plastic particles, with adverse consequences to marine foodwebs (Davidson 2012).
CAR-II	None		Ecological Impact	Habitat Change
In caging experiments at Maya Walk and Maya Alcove, Belize, exclusion of S. terebrans resulted in much more extensive growth and complexity of mangrove roots (Davidson et al. 2016).
EAS-III	None		Ecological Impact	Herbivory
Although Sphaeroma terebrans does not digest the roots of mangroves and other plants, the extensive boring of the roots of the mangrove Rhizophora mucronotata appears to limit the tree's distribution in the lower intertidal (Svavarsson et al. 2003).
EAS-III	None		Ecological Impact	Habitat Change
Although Sphaeroma terebrans does not digest the roots of mangroves and other plants, the extensive boring of the roots of the mangrove Rhizophora mucronotata appears to contribute to the disintegration of collapse of trees in the lower intertidal. This may limit the extent of an important habitat for terrestrial amd marine biota (Svavarsson et al. 2003).
NWP-3a	None		Ecological Impact	Herbivory
Although Sphaeroma terebrans does not digest the roots of mangroves and other plants, the extensive boring of the roots of the mangrove Rhizophora stylosa, and of the pneumatophores of Avicennia marina appears to limit the trees' distribution in the lower intertidal (Davidson et al. 2014).
NWP-3a	None		Ecological Impact	Habitat Change
Although Sphaeroma terebrans does not digest the roots of mangroves and other plants, the extensive boring of the roots of the mangrove Rhizophora stylosa, and of the pneumatophores of Avicennia marina appears to limit the trees' distribution in the lower intertidal (Davidson et al. 2014). This may limit the extent of an important habitat for terrestrial amd marine biota.
EA-III	None		Ecological Impact	Herbivory
Although Sphaeroma terebrans does not digest the roots of mangroves and other plants, the extensive boring of the roots of the mangrove Rhizophora mucronata appears to limit the trees' distribution in the lower intertidal (Davidson et al. 2014).
EA-III	None		Ecological Impact	Habitat Change
Although Sphaeroma terebrans does not digest the roots of mangroves and other plants, the extensive boring of the roots of the mangrove Rhizophora mucronotata appears to limit the trees' distribution in the lower intertidal (Davidson et al. 2014). This may limit the extent of an important habitat for terrestrial and marine biota.
FL	Florida		Ecological Impact	Habitat Change
Extensive damage to roots of Red Mangrove (Rhizophora mangle) was found with 80-100% of mangrove roots infested, and 30-60% of roots severed (Conover and Reid 1975)., Extensive damage to roots of Red mangrove (Rhizophora mangle) was found with 70-80% of mangrove roots infested, and 20-40% of roots severed (Conover and Reid 1975). In caging experiments in Rookery Bay (Bear Creek and Environmental Learning Center) and Braden River, exclusion of S. terebrans resulted in much more extensive growth and complexity of mangrove roots (Davidson et al. 2016). Extensive burrowing was also found in tidal brackish and fresh marshes, in peat and roots of Juncus plants. Burrows were especially common on the scarps of receding marshes, and could be accelerating marsh retreat (Estevez 1994). Boring by S. terebrans in plastic foam floats contribute to pollution by plastic particles, with adverse consequences to marine foodwebs (Davidson 2012)., Extensive damage to roots of Red Mangrove (Rhizophora mangle) was found with 80-100% of mangrove roots infested, and 60-100% of roots severed (Conover and Reid 1975). However, in experiments, R. mangle responds to boring activity by increasing the number of root endings in unparasitized roots, mostly those already buried in soil. Sphaeroma's boring activity could actually increase the stability of shorelines Simberloff et al. 1978; Ribi 1982)., Extensive damage to roots of Red Mangrove (Rhizophora mangle) was found with 100% of mangrove roots infested, and 80-100% of roots severed (Rehm and Humm 1973; Conover and Reid 1975). In caging experiments in Rookery Bay (Environmental Learning Center, Bear Creek), exclusion of S. terebrans resulted in much more extensive growth and complexity of mangrove roots (Davidson et al. 2016)., Extensive damage to roots of Red Mangrove (Rhizophora mangle) was found with 80-100% of mangrove roots infested, and 20-80% of roots severed (Conover and Reid 1975)., Extensive damage to roots of Red Mangrove (Rhizophora mangle) was found with 100% of mangrove roots infested, and 90% of roots severed (Conover and Reid 1975)., Extensive damage to roots of Red Mangrove (Rhizophora mangle) was found with 70% of mangrove roots infested, and 20% of roots severed (Conover and Reid 1975)., Extensive damage to roots of Red Mangrove (Rhizophora mangle) was found with 100% of mangrove roots infested, and 80-100% of roots severed (Conover and Reid 1975)., Extensive damage to roots of Red Mangrove (Rhizophora mangle) was found with 90-100% of mangrove roots infested, and 50-80% of roots severed (Conover and Reid 1975)., Extensive damage to roots of Red Mangrove (Rhizophora mangle) was found with 90% of mangrove roots infested, and 60% of roots severed (Conover and Reid 1975).
FL	Florida		Economic Impact	Shipping/Boating
Sphaeroma terebrans has caused damage to docks, pilings, and boat hulls (Atwood 1920). Damage to plastic floats was extensive in southwest Florida and in Lake Pontchartrain LA (Davidson 2012).

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