Branching Bryozoa and Red Algae

Bugula neritina and Neosiphonia harveyi

One of the issues facing a biologist out in the field when trying to identify marine species is matching the photographs in guides with what is seen with fresh material.  Guides do not give examples of all the different morphological or color variants.  Nor do they show the appearance of species at different ages (sizes) or stages of the life cycle.  In my experience, an unfamiliar species may require a few occasions to sort out the distinctions.  This was the case for me with Bugula neritina.  It has an algae-like, bushy growth pattern and is sometimes not abundant enough to form an immediate identification.  Using a 30x or 40x hand lens in the field or bringing samples back to the lab for microscopic confirmation have been a big help.  In due time, the identification process gets refined.

Among the red algaes, Neosiphonia harveyi is one species that can cause confusion when attempting to identify Bugula neritina, especially when the specimens are young (only a few cm in height) and neither of them has developed reproductive structures.  Side by side in a collection tray, the macroscopic differences can be easily discerned.  Under a microscope, however, the structural differences are crystal clear.  Bugula has serrated edges and  alternating biserial growth.  It is an animal with moving, feeding lophophores that contract down into their enclosures at the slightest disturbance and then slowly reappear to resume feeding (very entertaining).  Neosiphonia is a plant that has smooth, striped, non-moving branches (thalli) with pointed tips.  Each of the two species has unique, visible reproductive structures.  Bugula has white ovicells along mature branches, whereas Neosiphonia has pod-like carposporangia, both of which can been seen with the naked eye or hand lens.

Neosiphonia harveyi, previously classified as Polysiphonia harveyi (Choi et al, 2001), is a multicellular red alga with two macroscopic phases to its life cycle: a haploid, reproductive structure that produces gametes and a diploid form that produces spores for asexual reproduction.  The multicellullar branches in both stages of Polysiphonia and Neosiphonia species are composed of 5 primary cells in cross section, one central and 4 peripheral (see Algaebase link below).  Both stages look the same, i.e. they are isomorphic, and in Neosiphonia, the male and female structures are produced on the same plant.    

Bugula neritina and Neosiphonia harveyi with Similar Appearance and Size 

Wine red specimens of Bugula neritina (left) and Neosiphonia harveyi (right) collected from MacMillan Wharf in Provincetown, September, 2012.  Both the bryozoan and red alga branch with a similar bifurcating pattern, but branches of Bugula appear thicker and serrated.  Neosiphonia has a filamentous appearance but is actually composed of multicellular thalli (red algal fronds).  Neither specimen has conspicuous reproductive structures.

Microscopic View of Terminal Branches of Bugula neritina

Alternating zooids along the branch of Bugula with a cluster of feeding lophophores at the terminal end.  Each branch is two rows of zooids wide.  Serrated edges and alternating zooids can be with a hand lens.  Lophophores can also be seen with a lens on resting colonies in a shallow dish.  Stereozoom 4 x 10x objective.

Microscopic Views of Thalli of Neosiphonia harveyi

 Specimen was collected from Provincetown, September, 2012.  The segmented branches have red longitudinal and inter-segment bands. This structure can be seen with a 30x hand lens.   Branch ends taper to a tip.  Stereozoom 4.5 (upper) and 4.0 (lower) x 10x objective.

 

Neosiphonia harveyii Thalli with Carposporangia

 Specimen was collected from Wellfleet, July, 2011.  Carposporangia containing the newly fertilized (diploid) carposporophyte are located on short branches off the thallus.  The carposporophyte produces carpospores which are released into the sea water. 

Neosiphonia harveyii Growing as an Epiphyte on Grateloupia turuturu

Neosiphonia harveyi can be found growing as an epiphyte on several different algae.  Here it is seen on the MIS invasive species Grateloupia turuturu, which is becoming more common in the Gulf of Maine, especially in late summer.  From MacMillan Wharf, Provincetown, September 2012.

LINKS:

MarLIN: The Marine Life Information Network, Biodiversity & Conservation.  Descriptions of major taxonomic groups.  

The life cycle of red algae involves the alternation of three stages: the gametophyte, the carposporophyte, and the tetrasporophyte.  Typical red algae have separate male and female gametophytes, but Neosiphonia has both on the same plant.  The carposporophyte is microscopic and attached to the gametophyte.

WoRMS: World Registry of Marine Species.  Neosiphonia harveyi (J.W.Bailey) M.-S. Kim, H.-G. Choi, M.D. Guiry & G.W. Saunders, 2001. 

Algaebase.  Neosiphonia harveyi (J.W. Bailey).  Database of information on algae, especially marine algae.

Colorized cross section through a thallus showing cellular structure.

Plant Physiology Information Website by Ross E Koning: Kingdom Rhodophyta: Neosiphonia harveyi.  The life cycle is described and well illustrated.

Carposporangia on haploid plants contain a microscopic diploid carposporophyte after fertilization.

Marevita (Sea Life) - Algues et Plantes Marines - Rhodophyta:  Neosiphonia harveyi. 

 

Tetrasporangia spiral along the diploid thallus.  Carposporangia are produced on short stalks off the haploid thallus. (Photo credit: Andre Rio)

PUBLICATIONS:

Choi, H-G, M-S Kim, MD Guiry, and GW Saunders. Phylogenetic relationships of Polysiphonia (Rhodomelaceae, Rhodophyta) and its relatives based on anatomical and nuclear small-subunit rDNA sequence data. Canadian Journal of Botany 79: 1465-1476, 2001.

Morphological features of the A) thallus, B) rhizoid, C) carpogonium D) spermatangia, and E) tetraspores of i) Polysiphonia, iii) Neosiphonia, and ii) a multicentral relative.

Phylogenic relationships and reclassification of Polysiphonia harveyi as

Neosiphonia harveyi based on morphological criteria

Mathieson AC, JR Pederson, CD Neefus, CJ Dawes, and TL Bray.  Multiple assessments of introduced seaweeds in the Northwest Atlantic.  ICES Journal of Marine Science, 65: 730–741, 2008.

MIS Branching Bryozoan

Bugula neritina

Bryozoans are tiny colonial invertebrates that feed with a tentacled structure called a lophophore that filters food particles out of sea water.  Bryozoan colonies grow either laterally as broad encrusting mats or vertically as upright, branching bushes.  In the Gulf of Maine, encrusting species include the MIS invasive species Membranipora membranacea (February, 2012) and the native Electra pilosa (March, 2012).  Several upright, branching Byozoan species can also be found, including several beige native species of Bugula (e.g., Bugula simplex and Bugula turrita) and the wine-red Pacific coast species Bugula neritina, which is commonly found in floating dock communities (October, 2012) growing among algae and other invertebrates.

The branching colony is formed by the upright growth of feeding individuals called zooids that are enclosed in a calcareous box called the zooecium. Each branch of the colony is made up of a double row of zooecia and all the zooecia face in the same direction. The two rows in a branch are staggered, so that the top of one zooecium comes to about the middle of the one next to it. A single zooecium has a flexible membrane, and it bears no spines, although the upper, outer corner of the zooecium is pointed. Other species of Bugula bear distinctive, bird-head shaped structures with a jaw-like element that opens and closes, that are called avicularia. However, Bugula neritina has none. 

Underwater Photograph of a Colony of Bugula neritina

Bugula neritina with purplish-red color showing branching pattern of the colony.  The branches have serrated edges from alternating zooids and bifurcate at regular intervals resulting in a uniformly branching structure.

Microscopic View of Zooid Lophophores and White Ovicells

Microscopic view of Bugula neritina showing translucent red zooids and numerous white ovicells.  Zooids and ovicells face toward the front.  The flaring, wine-glass-shaped  lophophore has 23 tentacles that are arranged around the mouth.  Each zooid produces a single embryo at a time, which is brooded in the ovicell. The ovicells are conspicuous and often abundant, appearing as numerous small white beads concentrated in the mature parts of the colony.



  

Diagram of a Generalized Branching Bryozoan showing Anatomy of the Zooid

Diagram of an upright bryozoan showing the relationship between the anatomy of the zooid and the exoskeletal branches.  The lophophore tentacles are covered with cilia arranged along the inner faces and sides. When feeding, the lophophore is fully extended.  Currents produced by the beating of the cilia carry food particles (primarily microscopic plankton) down along the tentacles to the mouth.

Diagram of Feeding (left) and Retracted (right) Upright Bryozoan  

Mechanism of feeding and retraction by upright bryozoans.  When feeding, the lophophore is fully extended and moves around in the water.  The body remains inside the enclosure.  When disturbed, the lophophore rapidly closes into a tube and the retractor muscles attached to the base of the lophophore pull the zooid into its enclosure. 

Diagram of the Life Cycle of an Upright Bryozoan 

The life cycle of an upright bryozoan.  Bugula neritina zooids are hermaphroditic. Zooids release eggs around the middle of their lifespan but don't release sperm until near the end, thus preventing self-fertilization.  When released from the ovicell, the non-feeding larvae settle onto hard surfaces within a few hours and metamorphose into the adult form. The initial upright feeding zooid, called the ancestrula, buds off other feeding zooids (autozooids), which in turn bud off others, enlarging the colony. The base of the colony forms a tubular holdfast with specialized non-feeding zooids (heterozooids) that attach to the substrate and also generate new branches. 

 Branch of a Young Colony of Bugula neritina 

A single branch of Bugula neritina like the one shown in the life cycle diagram above. A few ovicells can be seen on branches on the right side of the colony.  A short, second branch is growing from the holdfast.  

Diagram of the Branching Patterns of Bugula species   

Diagram of three different biserial branching patterns found in Bugula species as seen from the basal (rear) side.  Left, Branching with no transitional zone.  Middle, branching with a single transitional row of 4 zooids.  Right, branching with 2 transitional rows of 4 zooids before returning to biserial growth.

Scanning Electron Micrograph of a Branch of Bugula neritina 

SEM view of the exoskeleton of a branch seen from the front side.  With the soft tissues and frontal membranes removed, the interior spaces of the enclosures can be viewed.  Bugula neritina lacks spines but has a pointed outer corner that is well-illustrated by the zooecia on the left branch.  

Photograph of Bugula neritina Collected in Provincetown

 Two wine-red color variants of Bugula neritina collected from MacMillan Wharf in September, 2012.  Most of the colonies on the docks were 2-3 cm in height indicating that the larvae had settle during a similar period of time earlier in the summer.

Stereomicroscopic Image of Feeding Zooids with Lophophores Extended

 Stereomicroscopic view of several terminal zooids from a colony collected in Provincetown.  The zooids have wine-red lophophores.  The blue-orange lophophore is a double-exposure image of a zooid in motion.  Individual zooecia are clearly seen alternating along the branches.  Stereozoom 4.0 x 10x objective. 

Photograph of Beige Bryozoan Species Collected in Provincetown  

Beige bryozoan species collected from MacMillan Wharf in September, 2012.  The beige colonies were approximately the same size as the red colonies.  The colony was not identified down to species. The native Bugula simplex is a common bryozoan and is fan shaped but has thicker, triserially growing branches.  Bugula turrita grows in spiral whorls which are clearly evident when colonies are large.   [2018 UPDATE:  This species has been subsequently been identified as Tricellaria inopinata.]

LINKS: 

Guide to Marine Invaders in the Gulf of Maine:  Bugula neritina ID Card

The Exotics Guide, Non-Native Marine Species of the North American Pacific Coast:  Bugula nerintina

Smithsonian Marine Station at Fort Pierce:  Bugula neritina

WoRMS World Registry of Marine Species: Bugula neritina

PUBLICATIONS:

Winston, JE, and RM Woolacott.  Redescription and revision of some red-pigmented Bugula species.  Bull. Mus. Comp. Zool. 159: 179-212, 2008.

Ryland, JS, JDD Bishop, H De Blauwe, A El Nagar, D Minchin, CA Wood, ALE Yunnie.  Alien species of Bugula (Bryozoa) along the Atlantic coasts of Europe.  Aquatic Invasions 6:17-31, 2011. 

WEB PHOTO FAV:

Bugula neritina: Lovell and Libby Langstroth Collection at the California Academy of Sciences.

MIS Floating Dock Community

Ascidians Claiming Space

On my last visit to Provincetown, I obtained a nice photograph of an invertebrate marine floating dock community at MacMillan Wharf - a shaded section of a float that was facing north, under a dock overhang, that had ascidians and other invertebrates growing together.  The upper few inches lacked a border of algae along the waterline that is characteristic of sunny locations.  It was a scene of moderate growth, before the species had a chance to completely overgrow each other into a mass of organisms (an enlargment of the whole photo is showing in the footer at the bottom of the blog).

Community of Invertebrates Below the Water Line

Species that are easily identified in the photo or enlargements:

• Styela clava, one large individual 8-10 cm long cloaked in Didemnum vexillum and several smaller individuals about 3-5 cm long growing along the waterline.
• Didemnum vexillum - Beige areas on the float, growing over Styela and other species. Didemnum was less abundant in 2012 than 2011. This float was one location in the marina where Didemnum was well-established and living together with Diplosoma.
• Diplosoma listerianum - Grey-colored, flat colonies that grow on the float and over Styela.  Diplosoma was the the most abundant ascidian in Provincetown in 2012, growing on many surfaces that were dominated by Didemnum last year.
• Botrylloides violaceus - Various small colonies, some tiny, in at least 2 shades of orange. Present everywhere but usually in limited discrete colonies. 
• Botryllus schlosseri - A single colony can be seen in the enlargement below. 
• Bugula neritina - A single wine-red colony about 2 cm high in the left center, immediately below a light-orange Botrylloides.

  A single mosaic-patterned colony of Botryllus schlosseri (left bottom) and a row of 5 Styela individuals (right) line up along the water line.  The first 4 Styela have clean, brown tunics whereas the 5th one on the right is partly covered by Diplosoma.    
Palaemonid shrimp can also be seen in the photo with pairs of flash-induced "white-eye" of their normally black eyes. There are 5 pairs of eyes in the photo (1 on the left side of the large Styela and 4 lined-up on the right).  
This year, a few Palaemon elegans, an MIS shrimp with blue-banded legs that is spreading throughout the Gulf of Maine, were seen at MacMillan Wharf.

Measuring Salinity of Seawater

Bring along the Refractometer

Seawater in the world's oceans has a salinity of about 35 parts per thousand.  Although the vast majority of seawater has a salinity of between 31 and 38 ppt, seawater is not uniformly saline throughout the world.  Where mixing occurs with fresh water runoff from the mouths of rivers or near melting glaciers, seawater can be substantially diluted. The most saline water is located at areas where high rates of evaporation and low levels of precipitation, river inflow, and circulation result in salty water (e.g. the Mediterranean and Red Seas).  Seawater is primarily composed of the positive ions Sodium (Na⁺), Magnesium (Mg⁺), Calcium (Ca⁺⁺), and Potassium (K⁺), and the negative ions Chloride (Cl^-) and Sulfate (SO₄^-2).  

Table of the Relative Amounts of Salts in Seawater

The salinity of seawater is determined with a refractometer, a laboratory or field device for the measurement of any aqueous solution using its index of refraction.  They are commonly used in science, medicine, brewing, and beverage production.  A different kind of refractometer is needed for each application, including seawater salinity.  In clinical medicine, a refractometer is used to measure protein concentration in human fluids such as urine, and in the food industry, a brix refractometer is used to measure the concentration of sugar in beverages.  In marine aquarium keeping, a refractometer is used to measure the salinity and specific gravity of aquarium water.   A seawater refractometer can be obtained online from a biological research laboratory supply company or retail stores that sell salt water aquarium supplies.

Hand-Held Refractometer

This refractometer measures salinity from 0 to 100 parts per thousand.  Left, held like a telescope, a sample of seawater is placed in the chamber and salinity is determined on a scale seen through the refractometer eyepiece.  Right, view through the eyepiece.  Salinity is expressed as optical density on the left scale and parts per thousand (ppt) on the right. 

Salinity in marinas on monitoring trips during summers of 2011-2012 ranged from 32-35 ppt in Provincetown and 30-34 pp in Wellfleet. These readings are not unexpected since the outer Cape Cod is continually replenished by currents in the Gulf of Maine and by high tides that penetrate up into streams.  The Cape also has a limited supply of fresh water from run-off and streams in comparison to Boston Harbor (Wellfleet Marina is at the mouth of a small stream, Duck Creek, and several streams empty into other areas of the harbor).   

Salinity in the Outer Cape

LINKS:
Holmes-Farley, R.  Refractometers and Salinity Measurement:  Reefkeeping: An online magazine for the marine aquarist. 
Wiki Refractometer
Seawater Refractometer Model I, Model II, Model III 
ATC Natural Seawater Refractometer 

Identifying The Vase Tunicate

The Yellow Siphon Rings of Ciona intestinalis

The Gulf of Maine is home to several solitary ascidians with gelatinous bodies and translucent tunics.  These species may be difficult to distinguish from each other when individuals are very young, in masses of mature individuals growing in social groups, or when morphology is masked by overgrowth of colonial ascidians such as Didemnum vexillum or Diplosoma listerianum.  In Provincetown, the cryptogenic Ciona intestinalis and native Molgula sp. (probably manhattensis) are very common, whereas the invasive Ascidiella aspersa, which is common in other marinas along the coast, is less frequently seen. 

Ciona is best distinguished from Ascidiella and Molgula by its elongate, vase shape which is less prominent in small individuals, and it's lemon yellow siphon rings which are visible even when young. The siphon rings are also crowned with 8 orange pigment organs that are more subtle but can be discerned by close examination.  When the siphons close, muscles contract the rings and bring the pigment organs closer together at the bases of notches in the contracted opening. The pigment organs have an ocellus-like structure and probably function in light detection, although there must be additional receptors to detect light because individuals who have the siphons removed still grow towards the light.

 

Yellow Siphon Rings of Ciona intestinalis

Yellow Siphon Rings of Ciona intestinalis. From Adrian Gittenberger's Dutch Ascidians Homepage (www.ascidians.com).

 

 Orange Oral Pigment Organs and Yellow Siphon Rings of Ciona

Eight orange pigment organs are seen on these individuals and can be easily distinguished when the images are enlarged. (The Ciona look like they are wearing jackets of Didemnum vexillum).  Photo by Arne Kuilman. 

 Orange Oral Pigment Organs

Partially closed siphons with orange pigment organs brought

closer together at notches of the contracted opening.

  

During the process of researching images and information on the siphon rings, I came across a 2010 paper on the structure and regeneration of the siphons that was particularly interesting, filled with beautiful color photographs of the yellow rings and orange pigment organs, and available open access on the internet.

 

Auger, H, Y Sasakura, JS Joly, WR Jeffery.  Regeneration of oral siphon pigment organs in the ascidian Ciona intestinalis.  Develop. Biol. 339: 374-389, 2010 (Elsevier).

 

Auger and his research team examined oral siphon regeneration after surgical removal in Ciona intestinalis.  After removal, the oral siphon rapidly reformed (orange) oral pigment organs (OPO) at its distal margin prior to slower regeneration of proximal siphon parts. The pattern of 8 OPOs and siphon lobes was restored with fidelity after dissecting only the end of the siphon, but as many as 16 OPOs and lobes could be reformed after dissection at the base of the siphon (complete removal).  

 

The oral pigment organs, siphon lobes, and yellow pigment bands were the first structures to regenerate. The yellow pigment bands formed as extensions of the pigment organs, which grew together along the edge of the siphons. The rest of the siphon grew outward after the orange oral pigment organs and yellow pigment bands were formed.  They concluded that the pattern of oral pigment organ regeneration is determined by cues positioned along the longitudinal axis of the oral siphon.

 

 Anatomy and Histology of the Oral Pigment Band (PB) and Organ (OPO)

 Morphology of the oral siphon.  A, the tunic was removed and the pigment cells and muscles are clearly visible.  B, higher magnicaiton of yellow and orange cells.  D-E, the ocellus-like organs consist of receptor epithelials cells and an underlying cup-shaped aggregation of organge pigment cells.  OS, oral siphon; AS, atrial siphon; OPO, oral pigment organ; PB, (yellow) pigment band; RC, receptor cells; PC, pigment cells. 

 

PUBLICATIONS:

Hecht, S.  The photo sensitivity of Ciona intestinalis.  J. Gen. Physiol. 1: 147-166, 1918. 
Sutton, MF.  The regeneration of the siphons of Ciona intestinalis.  J. Mar. Biol. Assoc. UK.  32: 249-268, 1953.

Dilly, PN, and JJ Wolken.  Studies on the receptors in Ciona intestinalis.  IV.  The ocellus in the adult.  Micron, 4: 11-29, 1973.  
Chiba, S, A Sasaki, A Nakayama, K Takamura, N Satoh.   Development of Ciona intestinalis juveniles (Through 2nd Ascidian Stage).   Zool. Sci. 21: 285-298, 2004.

The Gulf of Maine

Created by the Glaciers - Regulated by its Currents



The Gulf of Maine is a large body of water in the Northwest Atlantic Ocean between Cape Cod, Massachusetts, and Cape Sable, Nova Scotia.  Cape Cod Bay, Massachusetts Bay, and the Bay of Fundy are all included within the Gulf.  The underwater features of the seabed were sculptured during the last ice ages 25,000 years ago when  sea levels were lower.  Glaciers scoured the earth and deposited rocks and rubble creating the current Northeast American landmass and several underwater banks (Georges, Browns, Jeffreys, and Stellwagen).  The Gulf is a semi-enclosed sea bounded to the south by Georges Bank and to the east by Browns Bank.  The coastline north of Boston is predominantly rocky due to the effects of glaciation, which stripped sedimentary soil away.  Georges and Browns Banks separate the Gulf from the warmer waters of the Gulf Stream.   Gulf of Maine waters are more strongly influenced by the Nova Scotia and Labrador Currents, making the Gulf waters significantly colder and more nutrient-rich than those found to the south.

 

Bottom Topography of the Gulf of Maine 

Bottom Topography of the Gulf of Maine.  The outer banks enclose several basins and shallow banks that were formed during the advance and retreat of the glaciers.  The Stellwagen Bank is probably an underwater extension of Cape Cod, is the site of the Stellwagen Bank National Marine Sanctuary, and is famous for whale watching.

 

Temperatures in the West Atlantic showing effect of the Gulf Stream

 The Gulf Stream brings warm water from the Caribbean north (red) along the Florida Coast and moves off the coast at Cape Hatteras.   In the summer, eddies and meanders from the Gulf Stream bring warm waters to the mid-Atlantic States and Long Island.  The Labrador Current brings cold water south from Nova Scotia to the Gulf of Maine.  Massachusetts and Cape Cod Bays form a transitional region between colder waters to the north and warmer waters from the Gulf Stream.

Sea Surface Temperatures Along the North American Coast 

Winter and Summer sea surface temperatures along the mid-Atlantic coast and in the Gulf of Maine.  In the winter, the Labrador Current pushes the warm waters from the Gulf Stream south and away from the Northeast coast.  In the summer, warm waters move north towards the Mid-Atlantic States, but the Gulf of Maine remains cooler due to water flowing south from Nova Scotia into the Gulf.

 

Currents in the Gulf of Maine

Within the Gulf, circulation is strongly influenced by the Nova Scotia Current which brings nutrient-rich waters through the Northeast Channel. This current helps drive the primarily counterclockwise circulation of the Gulf which brings cooler water from Maine to Massachusetts. The main currents circulate around the basins, allowing shallow waters along the coast and in Cape Cod Bay to warm up during the summer.  The currents are also influenced by fluctuations in river outflow, often enhanced during spring runoff, and by huge tides (over 10 feet in Provincetown).  Tidal variation increases in a northeast direction along the coastsline reaching a maximum in the Bay of Fundy with variations over 50 feet.

 

 Representative Salinity Levels in Massachusetts and Cape Cod Bays

Salinity in the Gulf of Maine.  Five-day averaged surface salinity (color) and currents (cm s⁻¹) (arrows) during spring blood periods in 1998 and 2000.  Units given in parts per thousand.  Fresh water from rivers on the northeast MA coastline north of Cape Ann (upper dark blue area) and in Boston Harbor (lower dark blue area) reduce salinity levels at the source and locations south of the rivers (because of water currents in the Gulf of Maine, see above).  The outer Cape, including Provincetown, are less affected by rivers because the watershed is limited and large tidal variations recirculate sea water in the marinas.

 

River Systems in Boston Harbor and Coastline North of Cape Ann 

Left, North of Cape Ann, the Merrimack River empties directly on the Coast.  The Parker and  Ipswich Rivers empty into Plum Island Sound whereas the Essex River drains into Essex Bay. 

Right, in Boston Harbor, the Charles and Mystic Rivers empty into the north harbor, the Neponset River joins the mid-harbor at Quincy, and in the south harbor, the Weymouth Fore and Back Rivers empty into Hingham Harbor.  

 

LINKS: 

GOMA - Gulf of Maine Area: Oceanography/Circulation.

Ecology of the Northeast U.S. Continental Shelf: Oceanography

New England Coastal Wildlife Alliance: The Gulf of Maine

Stellwagen Bank National Marine Sanctuary

Jiang, M., Z. Meng, S. Libby, and C.D. Hunt.  Influences of the Gulf of Maine intrusion on the Massachusetts Bay spring bloom: A comparison between 1998 and 2000. Continental Shelf Research. 27: 2465–2485, 2007.