Corophium keeps a low profile; so low in fact that until a couple of decades ago the mudflats of Fundy were considered lifeless wastelands of little ecological interest. But as sandpipers have known for innumerable generations, and scientists have recently learned, if you probe beneath the surface, the mud is home to unbelievably large numbers of these tiny amphipods. To most of us a mudflat is a mudflat, and a rather boring, barren, lifeless, featureless expanse of real estate at that. But Corophium is more discriminating in its perception, and over the flat’s vast, unmarked expanse there are clearly desirable residential neighbourhoods and others to avoid. The salt content of the water washing over the flat is a minor consideration. Corophium can live in water saltier than seawater (~34 parts per thousand or "ppt." of salt) as well as in water only slightly saltier (~5 ppt. of salt) than freshwater, and readily tolerates everything in between. However, given the choice they tend to prefer, and thrive best at, a salt content around the middle of this range (~20 ppt. of salt).

Laboratory studies by Dr. Meadows in Wales shows that Corophium is "apparently quite deliberate" in choosing where it burrows. They aren’t simply attracted from afar to a particular area, but rather swim about at random, alighting occasionally to check out the surface. The colour of the substrate isn’t a concern, for they can pick out suitable sites even in the dark. Upon alighting, they crawl about and carefully manipulate particles of sediment, possibly to assess their texture and chemical characteristics. They respond to "some property of the surface layer of substrate when deciding whether or not to burrow". The average house-hunting Corophium is chiefly concerned about the size and nature of the sediment particles present in different parts of the mudflat. Ideally they should be of a particular size range, with just the right mix of silt, clay and sand; neither too finely silty, nor too coarsely sandy. It doesn’t mind a little blackish mud with low oxygen just beneath the surface. In fact, in the laboratory, if offered a choice it opts for sediments with reduced oxygen content. The size of particles is particularly important for the mud to have the right consistency for digging burrows. If it is too fine and watery, burrows can’t be built or soon collapse. If it is too coarse, less organic film is present on the surfaces of the large particles. Sediment particles must be small and well coated with such organic matter if they are to be acceptable as food. These natural slimy "biofilms" typically consist of bacteria, microscopic algae, fungi, protozoans and their secretions, as well as other organic compounds that stick to the particle surface. As we shall see, such biofilms are important as food; so Corophium is not just looking for a good stable home, but one with a well-stocked larder as well. In addition, the depth of the sediment layer must be at least ~0.5 cm, with larger animals requiring an even deeper layer in which to burrow.

The composition of the mud in different parts of a flat can vary greatly. Current or wave action may wash out fine particles in some areas, while elsewhere small depressions or channels may trap fine sediments and organic material. Mudflats thus tend to be a patchwork, and it is not surprising that the distribution and abundance of Corophium is also patchy. This makes it difficult to estimate numbers on a particular mudflat. The patchiness is further enhanced by the fact that Corophium likes to be close to its neighbours; the presence of other burrows is a bonus in site selection. In the laboratory, animals overwhelmingly preferred mud containing previously burrowed animals to mud without burrows. Interestingly, groups of animals burrowed readily, while isolated ones did not. In selecting sites, the animals also check the depth by probing the substrate with their elongated second antennae. If conditions are suitable they burrow and if not, they simply move off to investigate other sites.

Managing mudflats

Although some aspects of the reproduction of Corophium are still a mystery, we have learned a great deal. There are usually as many as four to ten times more females than males: what is termed a highly skewed sex ratio. Typically, it is the outnumbered males that initiate reproduction. On ebbing tides, in the short interval after the water has receded, when the sediment surface is still soft and wet, mature males emerge from their burrows and set off in search of a mate. Thanks to painstaking observations by researchers, such as Sherman Boates and colleagues affiliated with Acadia University, we have a clearer picture of these preliminary courtship rites. Far out on a mudflat, for an hour or two as the tide ebbed, these researchers hunched over the mud and diligently followed individual males crawling about in search of females. The amphipods tentatively investigated any burrows they encountered. At the mouth of each one examined, but not entered, the researchers dutifully planted a tiny, red flag. Eventually, after checking several burrows the male would find one to his liking and disappear inside. This burrow was marked with a green flag. As many as ten animals were followed in this manner on each tide. Before the tide returned, the researchers carefully dug up the patch of mud containing all the flagged burrows. They then teased apart the mud to collect the occupants of the burrows, recording the number in each, their sex and size, as well as the reproductive condition of females. In the course of 31 such trips to the mudflat they successfully tracked a total of 236 males and learned several interesting things. Most males visited from 2 to 6 burrows before finally entering one, although a few hard-to-please ones visited as many as 17 or 18 before committing themselves. Occasionally a roving male happened upon the home of another male, or one containing an already paired male and female. Such encounters inevitably led to conflict between the males in the course of which "the tube dwelling male and intruder interlocked their second antennae and the tube dwelling male pushed the intruder away from the burrow". However, many of the burrows visited did contain potential mates. To the researchers’ keen eyes, the "males definitely appeared to assess the females" stationed at the mouths of their burrows. They delicately ran their long antennae back and forth along the underside of the female, sometimes for three minutes or more. This caress may have helped determine the reproductive condition of the female, as males were much more likely to settle down with females on the verge of laying eggs. Surprisingly, given that larger females usually lay more eggs, the males didn’t seem to regard size as important in mate selection, as long as they were ready to lay. Once a male made his choice he moved into the burrow with his new mate. The females didn’t appear to be so discriminating, for there was "no clear rejection of males by females". However, on three separate occasions researchers saw "females grab a male and attempt to drag it into the burrow". They laconically concluded that these were "attempts by females to secure matings from males". They note that this is not surprising given that "one sex is a limiting resource".

The manner in which copulation occurs in Corophium has never been observed, because it takes place in the privacy of the burrow. However, it is undoubtedly similar to that of other less secretive amphipods. An amphipod’s strategy for bearing young is somewhat akin to that of marsupials such as the kangaroo, in that the eggs are deposited into a pouch-like brood sac or "marsupium". Here they are fertilised and develop until the young are old enough to fend for themselves. The marsupium is slung beneath the thorax and is formed by several leaf-like blades or "oostegites" that project inward from each side and overlap in the middle to form the basket-like structure that forms the floor of the marsupium. Typically, copulation occurs soon after a female has moulted. The male twists his abdomen around so that the tail fan, which is near where the sperm ducts open, touches the marsupium. Sperm is released into the water and is immediately swept into the marsupium on the currents produced by the pleopods. The pair separates and almost immediately eggs are released into the marsupium and are fertilised. Females can lay between 10 and 172 eggs, depending on her size, but the average is about 38. It is not clear why Fundy animals appear to lay more eggs than their European cousins. Females carrying eggs or developing embryos in the brood pouch are referred to as "gravid". Most females don’t become gravid until they are larger than about 6 mm in length, although ones as small as 5.4 mm have been found. The round eggs are initially creamy white and surrounded by a thin, flexible "egg membrane". Over a period of about two weeks the eggs divide repeatedly to form embryos in which limbs and eyes soon become visible. All the while, the steadily beating pleopods flushes well-oxygenated water around the developing young. Amphipods undergo "direct development", meaning that the egg hatches out a miniature version of the adult rather than an unfamiliar looking larva. During development, as many as a quarter of the eggs or embryos may disappear from the brood pouch, as a result of some simply dying and others falling out.

Once the embryos are fully developed they are ready to break free of the protective egg membrane. They do this with the aid of "hatching spines" which are two to four sharp projections located on the top edge of the tail segment (telson). Curiously, these are not present on the first embryonic exoskeleton, but are on the new exoskeleton developing beneath it. In effect, the tiny animal has to moult and hatch almost simultaneously so that the newly exposed hatching spines can make an initial tear in the egg membrane as the animal squirms vigorously. A final series of violent contractions are usually sufficient to free the animal completely from the torn egg. Newly hatched animals are a 1.0 mm long replica of the adult. Free-living animals of this size have been collected, suggesting that some leave the marsupium almost immediately. Most, however, remain inside for several days and may even moult again before finally launching out into the world.

Corophium are not finicky eaters, but the food must be of a suitable size. They can feed on particles lying on the seafloor (deposit feeding) as well as on ones suspended in the water (filter feeding). To deposit feed, they partly emerge from the burrow and use the large second antennae as rakes to pull particles towards the mouth of the burrow. Currents produced by the beating pleopods draw in this light, loose material. Some of the feeding limbs, the gnathopods, have long, fine bristles or "setae" which overlap to form a filtering basket through which the water passes. Particles larger about 0.004-mm are trapped on the mesh. Other feeding limbs deftly comb the particles off the mesh, sorting out the desirable ones and moving them forwards to the mouth. Here they are crushed between the grinding mandibles and swallowed. Essentially the same procedure is used to strain out any food particles suspended in the water flowing through the burrow. The pleopods may pump between 25 and 100 ml of water per hour through the burrow, bearing both food and oxygen. After a period of feeding at one opening, the animal withdraws into its burrow and may either rest or dextrously turn around in the narrow confines and emerge headfirst to continue feeding at the other entrance. They deposit feed at any stage of the tide and no daily cycle in their dining is evident.

Corophium may pick at their food, but they certainly don’t dawdle over it. An actively feeding animal can fill its stomach in about half an hour and digestion takes less than an hour. Examination of their stomach’s content offers little insight into the diet of Corophium. Typically less than 1% of the material is identifiable under the microscope, a tribute to the grinding efficacy of the tooth-like mandibles. Bottom deposits and seawater contain a variety of potential food particles of a suitable size (0.004 to 0.060mm). In summer, the most important are cells of single-celled plants or "diatoms" that flourish on the damp surface of the mud ("benthic"). A single animal may consume as many as 4000 diatoms a day. In a year, the Corophium population could consume more than a quarter of the total benthic diatom production of a given area. Decaying fragments of plant material or "detritus", wash off nearby salt marshes onto the mudflats, particularly in the spring and fall and supplement their diets when diatoms are scarce. But a limited ability to digest the plant detritus suggests that they may be feeding mostly on the bacteria growing on it. Bacteria seem to be an important food source so long as they are attached to particles larger than about 0.004 mm; because by themselves they readily pass through Corophium’s filtering mesh. They inevitably ingest a large amount of fine sediment when deposit-feeding and the organic–rich biofilms coating the particles are probably digested during passage through the gut. They can also gnaw off the biofilms from larger particles using their mandibles in a process called "epipsammic browsing". Up to three-quarters of the diatom material, but only about a quarter of the bacterial material, is digested and absorbed. Lipid digesting (lipases) and protein digesting (proteases) enzymes are present in the stomach. Much lower amounts of cellulose digesting enzymes (cellulases) confirm that they can’t directly digest salt marsh detritus very well. The proportions of these digestive enzymes present in the stomach changes from season to season in accordance with the different foods available. Thus in spring Corophium may rely on the more abundant salt-marsh detritus and accompanying bacteria, while in summer they consume chiefly their preferred diatom diet.

When habitat conditions are right and food is plentiful, Corophium populations can attain incredibly high densities. On a productive mudflat there can be 10,000 to 20,000 animals per square metre (about the size of a beach towel). In some areas of Fundy, densities greater of 60,000 per square metre have been observed. But their numbers are not this high throughout the year. The intricacies of the life cycle and predation by birds and fish result in sharp seasonal peaks and troughs in abundance. However, not all populations follow exactly the same patterns. In the upper Bay of Fundy, two distinct generations are produced each year. In contrast, in the outer Bay, around and below Saint John, N.B., there is only one annual generation. This is thought to stem from the colder average temperature (~6°C) that prevails there. A similar phenomenon occurs in European waters, with single generations in colder northern areas and two in warmer southern climes.

Corophium faces many perils on its deceptively benign-looking mudflat. An increasing number of these threats bear the imprint of human handiwork, but most are quite natural. Corophium is high on the menu for a wide range of hungry animals. As the rising tide washes over the mudflats, schools of small fish such as tomcod, flounder, smelt and mummichogs, which have waited expectantly just beyond the surf, scurry in over the newly submerged bottom in search of a meal. That this muddy larder is well-stocked is evident from the fact that on the other side of the tide line equally numerous flocks of hungry shorebirds, such as sandpipers, plovers and other waders impatiently await their turn at the same table once the water recedes. Corophium is the main course at both these intertidal banquets. Not much is known about the predation by fish and the effects on the Corophium population, because it occurs hidden beneath the waves. A great deal more is known about the effects of predation by birds, thanks to the decades of intensive studies by Peter Hicklin of the Canadian Wildlife Service in Sackville New Brunswick and Sherman Boates, of the Nova Scotia Department of Natural Resources. Both launched their initial research on Corophium while students at Acadia University.

The annual onslaught by the hungry shorebirds is intense (2-3 million birds, each eating from 10 to 20 thousand Corophium during a single tidal cycle) but relatively brief (about 6 weeks, in late July and early August; although individuals remain only for the 10-15 days needed to double their weight). Researchers think that this highly focussed, short-term attack alters not only the size distribution of the prey but also their population dynamics and possibly even their genetic characteristics. The mudflats at Starr’s Point and Blomidon in the Minas Basin, near Acadia University, are providing an ideal natural laboratory for studying the effects of such heavy predation. The sandpipers feed intensively on Corophium at Starr’s Point. However, only 10 km away at Blomidon, very similar mudflats are largely unvisited, because the high tides wash right up to the steep cliff face, leaving no beach for the birds to roost on while they wait for the tide to turn. The exact nature and ecological implications of the interesting differences in the life history of the Corophium populations at the two sites are only now being explored.

Some of the differences are undoubtedly linked to the fact that the sandpipers are rather choosy as to which Corophium they eat. They clearly select the larger ones, particularly the larger males, which thus bear the brunt of predation. As we have seen, these are the very animals that come out of their burrows as the tide recedes, to scout the mudflat for mates. The sandpipers have learned that by following the receding tide down the flat they will find an abundance of large, amorous amphipods right on the mud surface – easy pickings! But it seems that the amphipods somehow recognise the danger that they are in, for within days of the arrival of the sandpipers, the number crawling on the surface decreases by more than 95%. There are still lots of large males burrowed in the mud, but somehow they sense that sandpipers are on the prowl and simply stay indoors. The sandpipers then have to resort to probing in the mud, where they still seek out the larger adults. Primarily eating the adults is a wise strategy from the bird’s point of view, because it is the uneaten juveniles that will live through the winter and produce the spring brood that will become their sustenance on their trip south the following year. The adults on the other hand are nearing the end of their life, having done their reproductive duty. By consuming them in large numbers the birds may be freeing up valuable habitat space and reducing competition for burrows and food, allowing the juveniles to grow more rapidly once the sandpipers have departed.

But marauding birds aren’t the only threat that Corophium has to worry about. Their habit of dwelling in the surface layers of intertidal, estuarine sediments makes them vulnerable to exposure to a variety of noxious or toxic materials that are washing into the marine environment. Many studies have demonstrated the animal’s sensitivity to some of these substances, such as organic wastes, pesticides, crude oil, heavy metals and PCB’s (polychlorinated biphenyls). These often bind to sediment particles and tend to accumulate in mudflats where they can be ingested or absorbed by the species living there. Corophium is sufficiently sensitive to some of these compounds to warrant being designated by Environment Canada as a standard test organism for assessing how toxic contaminated sediments are to marine life. Many of these compounds are ubiquitous in the marine environment, so it is not surprising that they have been detected in the habitat and tissues of Corophium in many places. At present the concentrations of most such compounds in the mudflats of the upper Bay are low and pose little threat to Corophium. The same cannot be said of mudflats located in estuaries that are dominated by large urban or industrial centres, such as near the city of Saint John, New Brunswick, or adjacent to large aquaculture operations, such as those in and around Passamaquoddy Bay.

Not only may Corophium itself be threatened by the build-up up of contaminants in the sediments, but its burrowing activities may increase the risk of exposure for many other organisms as well. By intensely reworking the surface layer of contaminated mud (a phenomenon known as "bioturbation") Corophium increases not only the amount of suspended matter in the overlying water but also the concentration of the contaminants that are bound to it. This makes the contaminated particles more accessible to animals that feed by filtering the water, such as mussels. The more amphipods there are in an area, the greater the transfer of contaminants to filter feeders. Thus, Corophium can play a significant role in transferring toxic substances buried in bottom sediments into the aquatic food chain.

Perhaps the most worrisome of the threats presently facing Corophium populations are changes in sediment dynamics and mudflat composition. It is suspected that some of the changes may be long-delayed effects of the blockage of most large rivers flowing into the Bay of Fundy by causeways over three decades ago. Additional changes in sediments may result from the already implemented and proposed experimental openings of tidal gates in some causeways. The nature of such sediment changes and the threats that these may pose to the ecosystem are discussed at greater length in Fundy Issues Number 3, "Sandpipers and sediments: shorebirds in the Bay of Fundy" and in Number 9, Dykes, dams and dynamos: the impacts of coastal structures".

A more immediate and localised threat to the habitat of Corophium comes from the widespread and intensive commercial harvest of bloodworms, Glyera dibrachiata, on the mudflats of the upper Bay. Large numbers of the worms are being exported for use as live bait in recreational fisheries, largely in the northeastern U.S. This "fishery" surged northward into the Bay after 1985, following the overexploitation and decimation of baitworm populations in New England waters. Harvesting involves manually turning over the upper 10-20 cm of mud with a fork-like rake. This not only destroys existing burrows, but also loosens the sediment, making it difficult to construct new ones. Large swaths of mudflat can be turned over during a single low tide by a small group of diggers. Such "ploughing" puts large amounts of sediment into suspension and destabilises extensive areas of intertidal mudflat. Corophium densities decline by as much as 40% on such areas. Juveniles are even more susceptible, for their numbers can be cut in half. This also has serious repercussions for the migrating shorebird populations, whose feeding ability can be reduced by two-thirds in these disturbed areas. These adverse effects on Corophium and shorebirds can persist for a year or more after harvesting ceases.

Natural processes can also physically disturb the mudflat habitat. In years when ice conditions are particularly harsh, large numbers of Corophium may be killed, not from the freezing, but from having their burrows destroyed by the ice. The surface of the mud can be deeply scoured and gouged by large, heavy chunks of ice moved around by tides, waves and currents. Sometimes this ice freezes into the mud surface at low tide and then floats off with layers of the mud attached as the tide rises. Major storms, usually prevalent in the autumn, can also kill large numbers of animals as a result of large waves washing away sediments and destroying burrows. Usually, after either harsh icing or storms, the populations recover by the following summer, with animals quickly recolonising from nearby undisturbed areas.

In some European estuaries, excessive amounts of dissolved nutrients adversely affected Corophium populations. Nutrients arising from domestic wastes or agricultural runoff stimulated an overproduction of seaweeds and other algae, a phenomenon termed "eutrophication". As we have seen, Corophium readily handles the tiny benthic algae or diatoms. But the larger algae such as Enteromorpha, or the sea lettuce Ulva, spreading across a mudflat can quickly wipe out a Corophium population. The constant sweeping of the seaweed fronds across the sediment surface disrupts the feeding of the animals and often entangles them. The high tidal flushing makes it unlikely that eutrophication will ever be a problem in most areas of the upper Bay of Fundy, although it could be occurring in estuaries near the mouth of the Bay, where blooms of Enteromorpha on mud flats are now often reported.

The Fundy Issues Series is an initiative of the Bay of Fundy Ecosystem Partnership. These publications describe our present scientific understanding of some of the environmental issues confronting the Bay. We hope that they will enhance your understanding of the biological richness and complexity of this unique marine area and the problems confronting it. Such awareness may encourage you to help in protecting it for the use and enjoyment of all, so that future generations may also share and appreciate its bounty and rare beauty.