Nippoleucon hinumensis

Invasion History

First Non-native North American Tidal Record: 1977
First Non-native West Coast Tidal Record: 1977
First Non-native East/Gulf Coast Tidal Record:

---

General Invasion History:

Nippoleucon hinumensis is native to the Northwest Pacific, and common in shallow bays and brackish estuaries. Available records from the native range are from Lake Hinimu, in the Ibariki Prefecture, on the Pacific coast of Honshu, Japan (Gamo 1967) and from Okayama Prefecture on the Seto Inland Sea (Akiyama and Yamamoto 2004a) and Gwangyang Bay, South Korea, on the Korea Strait (Lee and Lee 2003). In 1977, it was collected in Isthmus Slough, Coos Bay, Oregon (Carlton 1989), and in 1986, in the western Delta and Grizzly Bay, in the San Francisco estuary (Cohen and Carlton 1995). Currently, it ranges from San Francisco Bay to Puget Sound (Cohen and Carlton 1995; Cohen et al. 1998; Wonham and Carlton 2005), with at least one reported occurrence in southern California (Fairey et al. 2002).

North American Invasion History:

Invasion History on the West Coast:

Nippoleucon hinumensis was first reported from the West Coast in Coos Bay, Oregon (OR) in 1977 (Hancock et al. 1977, cited by Wonham and Carlton 2007; Carlton 1989). It was found in nearby Umpqua Bay in 1983 (Carlton 1989); the San Francisco estuary in 1986 (Cohen and Carlton 1995); Yaquina Bay, OR in 1988 (Carlton 1989; Castillo et al. 2000); the Columbia River estuary in 1994 (Sytsma et al. 2004); Tillamook Bay, OR in 1996 (Golden et al. 1998, cited by Cohen 2004); Grays Harbor, Washington (WA) in 1999 (Wilson and Partridge 2007); Puget Sound, WA in 1998 (Cohen et al. 1998), and Willapa Bay, WA in 2000 (Cohen et al. 2001). It was also collected in Tomales Bay, California (CA) in 2001 (Fairey et al. 2002), Bodega Bay, CA in 2011 (California Department of Fish and Wildlife 2014), and Port Hueneme, CA in 2001 (Fairey et al. 2002). This species burrows in sand, mud, and silt, and has reached very high densities in brackish parts of the San Francisco estuary (Cohen and Carlton 1995; Lee et al. 2003; Peterson and Vayssieres 2010), Coos Bay (Carlton 1989), and the Columbia River estuary (Sytsma et al. 2004).

It is common to abundant in polyhaline to oligohaline salinities, but in the San Francisco Delta region, it is most abundant during dry years (Lee et al. 2003; Peterson and Vayssieres 2010). Nippoleucon hinumensis swarms in the plankton at night for mating (Akiyama et al. 2004a), so has considerable potential for ballast water transport. It has also been reported from fouling plates (California Department of Fish and Wildlife 2014) and the hulls of cargo ships (Llansó et al. 2011), probably in sediment accumulating on fouled surfaces.

---

Description

Cumaceans have a somewhat tadpole-like appearance, with the head and thorax greatly expanded, and a long, tail-like abdomen. The carapace covers the first 3 thoracic somites (sometimes 4, and rarely 6), and forms a branchial cavity. The anterior margin of the carapace is drawn forward as pseudorostral lobes. The eyes are fused medially, but are on a median eyelobe which overlaps the base of the pseudorostral lobes. Most species lack a lens or pigment (including Nippoleucon hinumensis). The pereaon covers the posterior 4-5 thoracic segments, narrowing posteriorly. The abdomen or pleon consists of 6 segments, of which the 5th is the longest. Some species have a free telson, extending posteriorly between the uropods, but this is lacking in N. hinumensis.

In N. hinumensis, the anterior-ventral corner of the carapace is rounded. The carapace is about 1/5 of the animal's length. The first pereaon segment is wide, and easily seen in lateral view. The head bears five pairs of appendages. Antenna 1 is uniramous and lacks a conspicuous 'elbow'. As noted above, a telson is absent. The endopod of the uropod consists of two segments. Cumaceans, including N. hinumensis show sexual dimorphism in a number of features. The pseudorostrum projects further anteriorly in females than in males. In males, Antenna 2 lacks a brush of setae on peduncle articles 4 and 5, and peduncle segment 5 is subdivided by several rings, with each division having grasping teeth. Male cumaceans typically have a much longer antennal flagellum than females, often approaching body length, but in N. hinumensis, the male flagellum, while longer than the females, does not extend past the posterior margin of the carapace. The females have exopods on pereiopods 1-3, while males have exopods on pereiopods 1-4. Both males and females lack pleopods, while other male cumaceans may have several pairs. The holotype male specimen is 3.7 mm long; and the female paratype is 5.5 mm long. The description is based on: Gamo 1967; Barnes 1983; Watling 1991; and Watling 2007.

---

Taxonomy

Ecology

General:

Cumaceans are peracarid crustaceans which usually live buried in sand and mud in marine and estuarine waters. Sexes are separate and sexually dimorphic. Nippoleucon hinumensis, like other cumaceans, swarms in the water column during mating. Fertilization is internal, and young are brooded by the female. In populations in the Seto Inland Sea, Japan, males apparently die after mating, but females produced a second, and sometimes a third or fourth brood, indicating that sperm is stored after mating. Mating occurred in January-February, and the first brood was released in April. The first brood varied with size of the female, from ~30-78 eggs, but the second brood was smaller, 25-60 eggs. Most of the juveniles produced in the first brood undergo a summer diapause during the period of high summer temperatures (July-September), when feeding ceases (Akiyama and Yamamoto 2004a; Akiyama and Yamamoto 2004b). We do not know if this diapause occurs in West Coast populations.

Cumcaceans create a current and filter-feed on phytoplankton and detritus, and/or scrape microalgae and detritus from sand grains (Barnes 1983). Nippoleucon hinumensis inhabits muddy bays and estuaries at depths from the intertidal to at least 10 m depth (Akiyama and Yamamoto 2004a). It is tolerant of a wide range of temperatures, although most of the populations in the Seto Inland Sea undergo diapause during the warmer summer months (temperatures of ~28C) (Akiyama and Yamamoto 2004a). Nippoleucon hinumensis also tolerates a wide range of salinities, from polyhaline (18-30 PSU) to oligohaline waters (0-5 PSU); although it is abundant at low salinities only in dry years (Cohen and Carlton 2005; Lee et al. 2003; Sytsma et al. 2004; Peterson and Vayssieres 2010). Although N. hinumensis primarily dwells in muddy sediments, it can be abundant in the plankton (Rudy 2013) during nocturnal mating swarms, and has been collected on fouling plates (Fairey et al. 2002) and ships’ hulls (Llansó et al. 2011). Nippoleucon hinumensis is one of the dominant organisms in the San Francisco estuary, reaching peak densities of 12,000 m-3 and average densities exceeding 1,000 m-3 (Cohen and Carlton 1995; Lee et al. 2003; Peterson and Vayssieres 2010). It is one of the dominant foods of the introduced Mississippi Silverside (Menidia audens), an important forage fish, and is eaten in lesser quantities by the Yellowfin Goby (Acanthogobius flavimanus) and Western Mosquitofish (Gambusia affinis) (Howe et al. 2014).

Food:

Detrtius, microlalgae

Trophic Status:

Deposit Feeder

DepFed

---

Habitats

General Habitat	Unstructured Bottom	None
General Habitat	Salt-brackish marsh	None
General Habitat	Vessel Hull	None
Salinity Range	Mesohaline	5-18 PSU
Salinity Range	Polyhaline	18-30 PSU
Salinity Range	Euhaline	30-40 PSU
Salinity Range	Oligohaline	0.5-5 PSU
Tidal Range	Subtidal	None
Tidal Range	Low Intertidal	None
Vertical Habitat	Endobenthic	None
Vertical Habitat	Epibenthic	None

---

---

Tolerances and Life History Parameters

Minimum Temperature (ºC)	8	Field, Seto Inland Sea, Japan (Akiyama et al. 2004a).
Maximum Temperature (ºC)	28	Field, Seto Inland Sea , Japan(Akiyama et al. 2004a).
Minimum Salinity (‰)	0.7	Field observations, Fresh-Brackish-Muddy Zone (Delta, mean salinity 0.7 PSU, Lee et al. 2003)
Maximum Salinity (‰)	27.5	Field, mean salinity Marine-Muddy zone, South and Central Bays (Lee et al. 2003)
Maximum Length (mm)	5.5	Female paratype, Japan. The male holotype is 3.7 mm (Gamo 1967).
Broad Temperature Range	None	Cold temperate-Warm temperate
Broad Salinity Range	None	Mesohaline-Euhaline

General Impacts

Nippoleucon hinumensis reaches high abundances in some of the estuaries where it has been introduced, including Coos Bay, the Columbia River, and San Francisco Bay. Its ecological impacts have not been well studied, but it is potentially an important part of estuarine food webs, as a filter-feeder and food organism. In the San Francisco Bay Delta, it is an important prey item for an introduced fish, the Mississippi Silverside (Menidia audens) (Howe et al. 2014), and is probably a major prey item for other fishes and invertebrates.

---

Regional Impacts

NEP-V	Northern California to Mid Channel Islands		Ecological Impact	Food/Prey
Nippoleucon hinumensis is one of the dominant foods of the introduced Mississippi Silverside (Menidia audens), an important forage fish in Delta marshes. This cumacean was the most important prey numerically and in terms of nitrogen intake. It was eaten in lesser quantities by the Yellowfin Goby (Acanthogobius flavimanus) and Western Mosquitofish (Gambusia affinis) (Howe et al. 2014).
P090	San Francisco Bay		Ecological Impact	Food/Prey
Nippoleucon hinumensis is one of the dominant foods of the introduced Mississippi Silverside (Menidia audens), an important forage fish in Delta marshes. This cumacean was the most important prey numerically and in terms of nitrogen intake. It was eaten in lesser quantities by the Yellowfin Goby (Acanthogobius flavimanus) and Western Mosquitofish (Gambusia affinis) (Howe et al. 2014).
CA	California		Ecological Impact	Food/Prey
Nippoleucon hinumensis is one of the dominant foods of the introduced Mississippi Silverside (Menidia audens), an important forage fish in Delta marshes. This cumacean was the most important prey numerically and in terms of nitrogen intake. It was eaten in lesser quantities by the Yellowfin Goby (Acanthogobius flavimanus) and Western Mosquitofish (Gambusia affinis) (Howe et al. 2014)., Nippoleucon hinumensis is one of the dominant foods of the introduced Mississippi Silverside (Menidia audens), an important forage fish in Delta marshes. This cumacean was the most important prey numerically and in terms of nitrogen intake. It was eaten in lesser quantities by the Yellowfin Goby (Acanthogobius flavimanus) and Western Mosquitofish (Gambusia affinis) (Howe et al. 2014).

References

Aasen, Geir; Sweetnam, Dale A.; Lynch. Lisa M. (1998) Establishment of the wakasagi, Hypomesus nipponensis in the Sacramento-San Joaquin estuary., California Fish and Game 84(1): 31-35

Akiyama, T.; Yamamoto, Masamichi (2004a) Life history of Nippoleucon hinumensis (Crustacea: Cumacea: Leuconidae) in Seto Inland Sea of Japan. I. Summer diapause and molt cycle, Marine Ecology Progress Series 284: 211-225

Akiyama, T.; Yamamoto, Masamichi (2004b) Life history of Nippoleucon hinumensis (Crustacea: Cumacea: Leuconidae) in Seto Inland Sea of Japan. II. Non-diapausing subpopulation, Marine Ecology Progress Series 284: 227-235

Anttila-Huhtinen, Marja; Könönen, Katriina (2022) First records of the new non-indigenous species Nippoleucon hinumensis, Sahlbergia 28(1): 12-15

Barnes, Robert D. (1983) Invertebrate Zoology, Saunders, Philadelphia. Pp. 883

Cadien, Donald B. 2006 Comments on Cumacea for LH - Part 5. The Family Leuconidae. <missing URL>



California Department of Fish and Wildlife (2014) Introduced Aquatic Species in California Bays and Harbors, 2011 Survey, California Department of Fish and Wildlife, Sacramento CA. Pp. 1-36

Carlton, James T. (1989) <missing title>, <missing publisher>, <missing place>. Pp. <missing location>

Castillo, Gonzalo; Li, Hiram W.; Rossignol, Philippe (2000) Absence of overall feedback in a benthic estuarine community: a system potentially buffered from impacts of biological invasions., Estuaries 23(2): 275-291

Cohen, Andrew N. (2004) <missing title>, San Francisco Estuary Institute, San Francisco CA. Pp. 1-50

Cohen, Andrew N. and 10 authors (2005) <missing title>, San Francisco Estuary Institute, Oakland CA. Pp. <missing location>

Cohen, Andrew N. and 22 authors (2001) <missing title>, Washington State Department of Natural Resources, Olympia. Pp. <missing location>

Cohen, Andrew N.; Carlton, James T. (1995) Nonindigenous aquatic species in a United States estuary: a case study of the biological invasions of the San Francisco Bay and Delta, U.S. Fish and Wildlife Service and National Sea Grant College Program (Connecticut Sea Grant), Washington DC, Silver Spring MD.. Pp. <missing location>

Cohen, Andrew; and 16 authors. (1998) <missing title>, Washington State Department of Natural Resources, Olympia, Washington. Pp. 1-37

Fairey, Russell; Dunn, Roslyn; Sigala, Marco; Oliver, John (2002) Introduced aquatic species in California's coastal waters: Final Report, California Department of Fish and Game, Sacramento. Pp. <missing location>

Gamo, Sigeo (1967) Studies on the Cumacea (Crustacea, Malacostraca) of Japan. part I., Publications of the Seto Marine Biological Laboratory 15(2): 133-163

Grochowska, Maria (2006) Morphology of preimaginal stages ofLipara pullitarsis Doskocil & Chvala, 1971 (Diptera: Chloropidae)— a gall-forming fly in the common reed (Phragmites australis), Entomoloigica Fennica 17(1): 387-393

Howe, Emily R.; Simenstad, Charles A.; Toft, Jason D.; Cordell, Jeffrey R.; Bollens, Stephen M. (2014) Macroinvertebrate prey availability and fish diet selectivity in relation to environmental variables in natural and restoring North San Francisco Bay tidal marsh channels, San Francisco Estuary and Watershed Science 12(1): 1-46

Lee, Chang-Mok; Lee, Chyung-Sook (2003) A new record of genus Nippoleucon (Cumacea: Leuconidae) from Korea, Korean Journal of Systematic Zoology Molluscan Research 19(2): 257-265

Lee, Henry II; Thompson, Bruce; Lowe, Sarah (2003) Estuarine and scalar patterns of invasion in the soft-bottom benthic communities of the San Francisco estuary., Biological Invasions 5: 85-102

Llansó, Roberto J.; Sillett, Kristine; Scott, Lisa (2011) <missing title>, Versar, Inc., Columbia MD. Pp. <missing location>

Peterson, Heather A.; Vayssieres, Marc (2010) Benthic assemblage variability in the upper San Francisco estuary: A 27-year retrospective, San Francisco Estuary and Watershed Science <missing volume>: published online

Rudy, P. 2013 <em>Nippoleucon hinumensis</em> (=<em>Hemileucon comes</em>). <missing URL>



Sytsma, Mark D.; Cordell, Jeffrey R.; Chapman, John W.; Draheim, Robyn, C. (2004) <missing title>, Center for Lakes and Reservoirs, Portland State University, Portland OR. Pp. <missing location>

USGS Nonindigenous Aquatic Species Program 2003-2024 Nonindigenous Aquatic Species Database. https://nas.er.usgs.gov/



Watling, Les (1991) Revision of the cumacean family Leuconidae, Journal of Crustacean Biology 11(4): 569-582,

Watling, Les (2007) The Light and Smith Manual: Intertidal invertebrates from Central California to Oregon (4th edition), University of California Press, Berkeley. Pp. 495-503

Wilson, Sarah; Partridge, Valerie (2007) <missing title>, Washington State Department of Ecology, Olympia. Pp. 244

Wonham, Marjorie J.; Carlton, James T. (2005) Trends in marine biological invasions at local and regional scales: the Northeast Pacific Ocean as a model system, Biological Invasions 7: 369-392

---