The Biology of Partner Shrimps
Relationship to other Crustacea
Partner Shrimps belong to the Phylum Crustacea, Order Decapoda (meaning 10 legs) which includes the Shrimps, Crabs and Lobsters, of which there are about 10, 000 named species in many families. Partner shrimps are a type of Snapping Shrimp from the Family Alphaeidae. All are members of the genus Alpheus.
Morphology
Of the partner shrimp’s ten ‘legs’ the first two are the two conspicuous pincers at the business end. These may be referred to as nippers, major claws or first chelipeds. They are used for bulldozing, building coral rubble walls and stabilising the goby during cleaning by the shrimp.
The second pair of ‘legs’ are the less obvious slender clawed appendages lying just behind the big pincers. They are called the second chelipeds. They are used for fine manipulation of the algae these shrimps feed on and for maneuvering small fragments used in burrow construction. They are also used for cleaning the goby.
The remaining six legs are called the walking legs.
Behind these, on the underside of the animal are five pairs of paddle-like structures called pleopods and behind them, the scoop-like tail portion, called the uropod.
The body of the shrimp is encased in a hard shell, familiar to seafood eaters. At the front end is a spiky structure called the rostrum, beneath which are two long antennae and two shorter antennules. The shell itself consists of the carapace and a six-segmented abdomen terminating in the telson of the tail. The expanded lower portion of each abdominal segment is called the pleura.
Colour and pattern in Partner Shrimps
Certain aspects of design recur with varying degrees of prominence in different species of partner shrimps. Different designs result in species being recognisably different but with common features.
Among these common features are the presence or absence of diagonal bars on the side of the carapace, the presence or absence of a black patch on the side of the carapace and the intensity of a localised pale ‘epaulette’ on the side of the carapace, This last feature arises from the extension of the second of two semicircular pale crescents variably present on the top of the carapace.
Commonly modified designs on the abdomen include the presence of white bars on segments 1 and 4, longitudinal stripes, a line of spots along the lateral aspect, a single black spot on the side of segment 4, and transverse bars on each segment often making a rectangle with the longitudinal lines.
Pincers are helpful for the identification of species but follow a less predictable pattern, usually looking either marbled or barred, Legs are pretty standardised but the colour of the joints and the contrasting patch on either side can help differentiate species.
It is reasonable to infer a closer relationship between species that have similar patterns such as the Pyjama shrimps although their ecological requirements and relationships may be different
It is very important to be aware that the markings of a shrimp are always modified by features of the environment in which it is living.
The prime example of this is the difference seen in shrimps living on white sand and the same species in a black sand habitat. On black sand, there is an increase in the intensity and extent of dark pigment. This results in a change from a pale shrimp with scattered dark markings to a dark shrimp with scattered pale markings. It can be a little confusing but with any familiarity, it is pretty obvious that this is the same species. Incidentally, the same difference in appearance due to increased pigment is seen in the shrimpgoby partners, whose more complete taxonomy confirms that they are the same species.
Another example of environmental modification of colour is seen when the shrimp is feeding on large quantities of green algae. We have seen individuals become conspicuously green even when paired with a partner of the more usual brown colour.
In general colour and design are directed towards cryptic camouflage although some gaudy species have surprisingly effective disruptive camouflage. The strikingly pretty species like the Tiger Shrimp disappear against their usual habitat with variously coloured sand grains, an example of disruptive camouflage.
Even the dramatic colours of Randall’s Shrimp can be lost among the red and white shell fragments of coarse sand. It helps that the intervening portions of the body are transparent.
Many shrimp have designs that mirror the markings on their partner gobies. Common to both in some pairs is a pale body decorated with a line of darker lateral blotches. These match in colour and are patterned with similar fine squiggles. Of course, this may be a coincidence but, interestingly, animals of such different groups should evolve the same cryptic pattern out of all the possible choices.
Colour and design are difficult to see in silt-dwelling shrimp as they are almost always covered in silt. This gives them adequate camouflage anyway!
Reproduction
Male and female shrimps form permanent bonds and pairs share the same burrow. The female is bigger than the male at the same age with a broader abdomen and pleopods (Duerbaum 2012).
The whole reproductive cycle takes place within the burrow so it cannot be studied in the natural habitat.
Duerbaum (2012) has studied the mating sequence in a novel aquarium set-up. He found that the shrimps moult in the burrow every two to four weeks, always at night, and carefully chop up the exuviae and carry the pieces out of the entrance the next day. The pair mate after moulting and soon after the female can be seen carrying eggs on her pleopods. Ten days later the larvae hatch, again at night, and are washed out of the burrow, possibly by the beating of the pleopods.
Aquarium observations suggest that the female normally stays within an inner chamber until the eggs hatch. This is not the case on the reef. We have seen and recorded on video a female laden with eggs working along with the male excavating a channel near the burrow entrance. It has to be said that her activities were only moderately constructive.
Population replacement and density are not dependent on local reproductive success as the early stages of a shrimp’s life are planktonic Recruitment is usually from young shrimps that have arrived from elsewhere. Shrimps live for up to two years.
Predators of Shrimps
The main predators of shrimps are probably lizardfish, grubfish and flounders. The shrimps are very fast and the shrimpgobies, which sometimes look as though they are in a trance at the entrance are probably easier targets.
Parasites of Shrimps
It is not uncommon to see shrimps with swelling on one side of the carapace. This is made by a parasitic isopod (Bopyridae) living in the gill cavity or under the carapace of many species of shrimps and crabs.
Bulldozing technique
Partner shrimps have large flattened pincers that are used for burrow construction and maintenance. One pincer is always larger than the other. This may be the left or the right. The two pincers are used like the scoop of a front-end loader to lift and push a load of sand out and away from the burrow. The load is frequently so large that the shrimp is invisible from the front. To allow the shrimp to carry a larger load the pincers are often reinforced by a line of stiff bristles along the outer edge.
The pincers are asymmetrical, one being broad and flattened to work like a bulldozer blade and the other more rounded and suitable for manipulating large coral fragments. Fine manipulation of smaller pieces is the domain of the slender second cheliped. If a shrimp loses a pincer the second cheliped and first walking leg are brought in to replace it by steadying and manipulating shell and coral fragment as the burrow is constructed.
When a load of sand has been picked up inside the burrow the shrimp pushes it steadily out and away from the entrance. Most of the forward motion is achieved by the shrimp’s six walking legs, but when more grip is needed it drives itself forward using its pleopods. When the load is particularly heavy or the slope too steep the shrimp scrabbles so hard that it dislodges the sand under its pleopods and sends a stream of sand flying backwards into the burrow.
The shrimp may use this fact to its advantage by turning to face the burrow and using the pleopods to eject sand away from the entrance. This technique is particularly useful when the shrimp is working in loose sand where the grains tend to slide over each other. In this situation, the shrimp can be seen to enter the burrow head first before ejecting a stream of sand granules.
Larger pieces like bits of coral rubble or large shell fragments are not bulldozed away but carefully picked up in the pincers and stacked above the entrance in such a way that they are interleaved with similar fragments making a surprisingly stable wall. The shrimps display considerable strength and dexterity in this task. Some pieces are stacked nearby for later use in sealing off the entrance at night.
The burrow entrance is kept open as long as the shrimps are working. At night or when they are not working during the day the entrance is sealed. This is why a pair seen on a dive may not be seen there the next day.
If the goby on guard is in the way it is simply shoved aside by the shrimp as it goes through with its load. This tolerance of rough body contact is a testament to just how comfortable the partners are with each other.
Construction of the burrow
The exterior of the burrow
The visible portion of the burrow consists of a semicircular entrance of broken shell and coral debris, and often an open-topped channel 5 to 30 cm away from the entrance.
The channel allows shrimps and goby to forage further from the entrance without being visible from the side and creates a racetrack back to the burrow when a hasty retreat is called for.
The channel often terminates at a patch of algae. This is food for the shrimp. The pincers and clawed second legs are used to cut off and collect scraps that are eaten on the spot or carried back to the burrow for storage.
The channel is excavated by the shrimps working in pairs. This can be chaotic when the lead shrimp excavates too enthusiastically, reversing at high speed to pick up its next load just as the following shrimp emerges with its load!
When the channel extends more than an antenna’s length from the entrance the goby accompanies the shrimp rather like an owner being taken for a walk by his dog. Experienced gobies become very conscientious about this escort service and on occasion will initiate the move to venture further afield. Very young gobies tend to sit tight looking gormless. When this happens a large shrimp will pick up the small goby along with its load of sand and carry it along the channel until it gets the hang of the job.
The interior of the burrow
What we cannot tell from the surface is what the burrow is like beyond the entrance. Biologists have investigated this and found the burrow to be surprisingly extensive. The layout of burrows was studied by Yanagisawa (1984) by pouring resin down the entrance and digging up the cast when the resin solidified. Burrows of juvenile shrimps, by which we mean those that have settled on the sea bed 2 to 4 months previously, are 30 to 70 cm long, branched and may have offshoots leading to than one or more entrances. At this stage, the shrimps are small with a carapace length of 7 to 9 mm. The shrimps dig a burrow into the sand as soon as they settle. As the shrimps grow the burrow becomes deeper and more complex and burrows occupied by adult pairs are extensive, spreading to a distance of 100 cm and a depth of 70 cm. These have multiple entrances, different ones being used on different days and encompass a subterranean area of half to two square metres. Not surprisingly the area can overlap a neighbouring burrow. The tunnels are usually strengthened with coral rubble, shells and sand dollar skeletons.
Duerbaum (2012) carried out a beautiful study of the construction of the burrow in a specially set-up aquarium. The shrimps built the burrow along the glass base of an aquarium so he created a setup that allowed the whole of the underside of the tank to be monitored from below. Although two dimensional it allows fascinating insights into the behaviour of the pairs when out of sight in the burrow. His Tiger Shrimps, Alpheus bellulus, started excavating a burrow as soon as they were introduced into the aquarium. Within a few days, they had excavated a tunnel 60 cm in length. They then excavated side channels. Some of these became alternative burrow entrances and some were enlarged to make underground chambers. The shrimps moulted and mated in one of these chambers and a separate chamber was the centre of the goby reproduction.
Gobies can be clumsy as they move through the tunnels, often causing a collapse of the roof in the aquarium set-up. When this happened they would simply wait passively to be dug out by the shrimps.
Location of burrows
Burrows are not scattered randomly over the sea floor. They are distributed consistently according to local environmental factors important to the individual species of partner shrimp. Sediment characteristics, depth, and distance from the reef are all significant. The most important of these is the physical nature of the sediment.
The significance of sediment particle size
Substrate characteristics are critically important to the shrimps and are the chief determinant of their distribution. Silt particles stick together and make stable burrows, but it takes a bigger, more powerful shrimp to work it. Sand is less stable but can be manipulated by smaller shrimps. We will see later in this book that partner shrimps can be grouped by habitat into categories such as silt lovers, open sand lovers, sheltered sand lovers and so on.
Substrates may be considered as silt, fine sand, coarse sand, broken shells or coral debris. For interest here are some definitions.
Silt particles are between 0.002 and 0.063 mm in diameter and are usually mixed with vegetable matter. Sands consist of eroded rock or shell particles with diameters between 0.064 to 2 mm and are found in clearer water with more current or wave action. Fine sand has a diameter of less than 0.5 mm and coarse sand from 0.5 to 2 mm, after which the substrate is called gravel.
All partner shrimps are specialists in specific environments. For example, the Yellow Pyjama Shrimp is a coarse sand specialist. It doesn’t make a burrow in nice cohesive mud, but coarse sand is grist to its mill even though it tends to landslide unless mixed with shell and coral debris. The substrate found in sand gutters on the reef front is particularly loose and uncohesive. This is made up entirely of coarse shell and coral fragments because all the fine sand particles have been swept away over the reef flat. Even here the Yellow Pyjama Shrimp manages to construct burrows for the Burgundy Shrimpgoby, Amblyeleotris wheeleri.
So it might be expected that if you look for the appropriate substrate characteristics you will find the burrows equally distributed over the entire area. Of course, it is not as simple as that.
Even within a particular substrate zone, there is partitioning because currents and wave action sort sea bed particles of slightly different sizes into different layers horizontally and vertically. Each layer has its own ecological properties and supports different microbial animal and vegetable communities. The result is that the meiofauna, the tiny marine organisms that the gobies and shrimps depend on for food, is unevenly distributed.
This is probably why the horizontal distribution of shrimp gobies over an area of apparently uniform sediment size is so varied and unpredictable. It is not uncommon to find the only colony of a species occupying only a few square metres in the middle of an apparently uniform expanse of the sea floor.
Coarse sand habitat presents another problem. The larger particles tend to catch the current making the surface layer unstable with consequences for the burrow entrance and the ability of edible microorganisms to become established on the adjacent constantly rolling surface grains. The effect is made worse by strong currents.
The effect of current velocity and direction
Not surprisingly shrimp goby pairs thrive where there is good current carrying food and planktonic juveniles. This generally beneficial effect is strongly influenced by variations in current and seabed morphology.
If a sandy sea bed is free of projecting structures current flow is streamlined, therefore virtually stationary at the interface, and we see an even distribution of different species of shrimp-gobies and their shrimps,
Any structure, such as a rock outcrop, projecting into the water flow causes turbulence, creating downstream eddies that carry plankton and fine sand particles back into its lee. This creates an oasis of increased richness and many shrimp-goby pairs live almost exclusively close to rocks in coarse sand. Some carry this one stage further and live in small caves in current-swept coral reef drop-offs.
Sediment ripples caused by currents in places such as the reef front are unsuitable for burrows as they move and reshape like dunes. This is also true of areas densely colonised by burrowing worms or Callianassa sand prawns that make constantly changing pyramids of sand.
The influence of the oxygen gradient
Oxygen concentration in the sediment is greatest on the interface with the water and diminishes with depth but sediment characteristics modify this. Coarser sediments have larger spaces between grains and oxygen diffuses more readily through sand than fine silt, where conditions rapidly become anaerobic with depth. In these situations, one could imagine the burrow chambers being somewhat anoxic. Some goby species have greater tolerance of hypoxia and shrimpgobies and their shrimps may have an appropriate modification of their physiology. Observations in shrimpgoby burrows in an aquarium suggest that the goby maintains a flow of water through the burrow by finning.
The problems of burrows in shallow-water
We have found a remarkable situation at the Low Isles in far north Queensland. Two species of shrimpgoby, Cryptocentrus maudae and Cryptocentrus leucostictus, pair up with the Pale Marbled Shrimp and the Blue and Yellow Shrimp respectively in burrows near mangrove roots. These burrows are in extremely shallow water (20cm deep at median tide) so they are exposed for almost half of the time (tidal range up to 3 metres).
This seems to be a habitat with several disadvantages. Having the burrow exposed for part of the day is something that does not happen to other shrimpgobies as they live sub-tidally. The exposure leaves shrimpgobies vulnerable to dehydration as the tide goes out. The amount of time available for feeding is reduced to half tide and greater, which should mean halved but they are strictly diurnal fish so the nighttime high tide is not available. For much of that time, the water was extremely shallow, calm and exposed to the tropical sun. They need to tolerate a lot of heat stress.
How do they cope with this difficult environment? As the water level falls the shrimps block up the burrow entrance with coral pebbles. This camouflages the burrow when the tide is out and prevents access from the surface. It also must reduce the amount of drying out of the burrow. Enough water may remain in the burrow for the goby to remain submerged so it can still breathe. As you go deeper in the substrate it becomes increasingly anoxic and these shrimp and goby pairs must tolerate this. In a spring low tide, the sea surface level is more than a metre below the burrow entrance so the burrow would need to extend past this depth.
One must assume they occupy such a difficult niche because it has advantages that only they are physiologically adapted to exploit.