Environmentalenrichment Foraquaticanimals: Mike Corcoran
Environmentalenrichment Foraquaticanimals: Mike Corcoran
 KEYWORDS
  Fish enrichment  Fish medicine  Aquatic animal enrichment  Koi enrichment
  Tropical fish enrichment  Aquarium enrichment  Octopus enrichment
 KEY POINTS
  Enrichment decreases stress in captive animals and helps to promote natural behaviors.
  Effective enrichment programs decrease stereotypies and other abnormal behaviors.
  The basis for proper enrichment is proper husbandry, which includes excellent water qual-
   ity when discussing aquatic animals.
  Enrichment varies by species, age, and must sometimes be tailored individually.
  Training animals for medical procedures increases the effectiveness of medical treatment
   and decreases the associated risks for the animal and the staff.
The need for enrichment in captive animals is based on the fact that animals are capable
of experiencing pain, stress, and boredom. There are a number of peer-reviewed jour-
nal articles published even in recent decades that question these abilities in fish. As
such, this author feels that it is important to highlight some of the more recent publica-
tions and research debunking those old concepts so that readers have the more current
information at hand.
   Several arguments have been presented against the idea that fish have consciousness
or the ability to experience pain and suffering. The basis for these arguments was
the absence of a neocortex in fish. The assumption is that the neocortex is the center
of consciousness, and animals without a neocortex (such as fish) are unable to experi-
ence consciousness and, therefore, do not experience pain or suffering.1 More recent
work has shown this to be an oversimplified approach to the issue. Consciousness has
been linked with the thalamocortical system and is generated by a complex neural
      process rather than in a single region of the brain.2 In humans, the limbic system is the only
      area that consistently responds during perception of pain in imaging studies.2 Anatomi-
      cally, both A-delta and C fibers, which transmit pain, have been identified in the trigeminal
      nerves of fish. Stimulation of these nerves has been shown to stimulate areas of the brain
      involved in learning and emotion.2–4 The brains of teleost fish develop differently than
      mammalian brains. During embryologic development, the neural tube folds outward in
      fish, and inward in mammals. However, there are homologous areas of the fish brain
      corresponding with the hippocampus and amygdala in mammals, where emotion and
      learning take place.4 Comparing brain development, very conservative evolution has
      been observed among all vertebrates, with relatively similar brain function.4 Advances
      in the understanding of neuroanatomy and neurophysiology support the idea that fish
      are able to develop consciousness and experience pain.
         A second argument presented theorizes that, although aquatic animals respond to
      painful stimuli, they only react in a reflexive manner, with no understanding of the im-
      plications or emotional experience in association with the stimulus. Numerous studies
      have contradicted this theory. Trout injected with either acetic acid or bee venom had
      a significantly prolonged time approaching food compared with controls injected with
      saline. They also showed increased opercular movement and many rubbed the injec-
      tion site on the substrate. All of these changes were mediated when fish were given an
      injection of morphine before the noxious stimulus.4 Another study demonstrated that
      trout and goldfish both learned to avoid a specific region of a tank when that area was
      associated with an electrical shock. Interestingly, trout elected to remain in that region
      of the tank and be subjected to low-level electrical shocks when a conspecific was
      visible on that end of the tank. Goldfish remained near the middle of the tank when
      a conspecific was presented rather than retreating to the opposite end of the tank.5
      Both of these studies showed a clear difference in behavior based on a noxious
      stimulus. There was reduction of approach to a desired reward (food) or willingness
      to tolerate a noxious stimulus if offered socialization. Additionally, there was recogni-
      tion of the specific area of stimulation and an attempt to relieve discomfort by rubbing.
      This is not limited to fish. A study involving hermit crabs had similar results. The crabs
      were placed into 2 different types of shells. Previous studies demonstrated a prefer-
      ence of one over the other for hermit crabs. When an electrical shock was applied
      to the crabs, there was a significant difference in the likelihood of the crab evacuating
      the shell. Far more evacuated the less desirable shell compared with the other type.
      There were also observed acts of shock-related aggression toward the evacuated
      shell.6 Even if these studies do not clearly prove an emotional and conscious percep-
      tion of pain in aquatic animals, they do demonstrate behavior responses beyond
      reflexive withdrawal in response to noxious stimuli. This evidence should justify the
      need for minimizing pain for these animals.
         There has also been evidence of stress and fear demonstrated in fish. Acute stress
      from capture has clearly been associated with elevated cortisol and glucose levels in
      fish.3,7 Fear responses associated with imminent electrical shock in goldfish have
      been ameliorated with N-methyl-D-aspartate antagonists and fear responses associ-
      ated with an alarm pheromone in fish have been ameliorated with benzodiazepine
      treatment.3 Fish introduced to a novel environment show increased foraging behavior
      when treated with benzodiazepine medication.3 Restraint of some fish for 3 minutes or
      more decreased a behavioral pain response to injection of formalin. The behavior
      change was reduced if fish were pretreated with naloxone, demonstrating that the
      behavior change was owing to endogenous opioids released during acute stress
      from restraint.8 Studies in fish have demonstrated that subordinate fish experience
      chronic stress owing to the presence of dominant fish, regardless of the actual
                                            Environmental Enrichment for Aquatic Animals      307
aggressive behavior.3 Because one of the main objectives for enrichment is to alleviate
stress and encourage natural behaviors, it should be justified by these observations.
   The last argument to be presented in support of offering enrichment for fish
addresses the memory of fish. Most readers have probably heard the myth that by
the time a fish swims around its fish bowl that it has forgotten what it originally saw
in the bowl. In the latter sections of this article, training is discussed. The studies
and methods of training clearly show that fish are able to form long-term memories.
Nutrition
Nutrition for fish is complicated. Much of the research is focused on production fish
rather than ornamental fish, but much information can be extrapolated from that
research and applied to ornamental species. For a recent review of aquatic animal
nutrition, see the September 2014 issue of Veterinary Clinics of North America.
  Generally, protein levels should be 25% to 55% of the diet, depending on the
species.10–13 The protein source should be primarily animal proteins; fish meal is
best.12 Essential amino acids in fish are similar to those of other species, although
arginine is far more important for fish than for mammals.10,11 Fats should constitute
15% to 25% of the diet and fish require n-3 fatty acids.13 Fish oils are the best source
for the required fatty acids, and in general vegetable oils are a poor nutritional source
for aquatic animals.14 Carbohydrates are far less important to fish than to mammals.
Starches are more digestible than sugars and should make up about 10% of the diet.14
Most aquatic animal diets provide the needed vitamins so long as the diet is properly
stored. The foods should be protected from heat, light, and moisture and be used
within 6 months. Minerals are usually provided by the water directly and do not require
supplementation in the diet if water quality is good.10,13,14 See Fig. 1 for general ratios
of elements in the diet.
  With respect to enrichment, there are a number of options involving foods. The
specific diets for specific animals does require some knowledge of the species, at
least the type of environment it has in the wild and whether it is a carnivore, omnivore
or herbivore. Beyond that, some degree of variety is good for most species of aquatic
 Box 1
 Five freedoms of welfare for terrestrial farm animals (Farm Animal Welfare Council)
                                                                   Protein
                                                                   Fat
                                                                   Carbohydrate
                                                                   Fiber
Carnivorous Fish
                                                         Protein
                                                         Fat
                                                         Carbohydrate
                                                         Fiber
      animals. Again, there is not the degree of dietary knowledge for ornamental fish
      compared with that available for other domestic species. Offering a variety of foods
      within the general guidelines above can help to ensure that all nutrients are offered.
      Any nutrients missing from one diet can be made up for with others. Until long term
      nutritional studies can be performed on ornamental fish, this offers the best option
      for nutritional well-being. Keep in mind that many ornamental fish are still wild caught
      animals or 1–2 generations of captive breeding, so they do not have generations of
      selective breeding adapting them to conditions in captivity. While many canines and
      felines do not tolerate variation in diet, wild fish normally have a great deal of variety
      in their diets (depending on the species).
         Variations in the diet also offer novel stimulation for psychological well-being.
      Commercial fish diets come in a wide range of formulations: live food, liquid diets,
      frozen diets, flakes, pellets, and gels. Among these there are also variations in size,
      shape, and color. Pellets can either be formulated to float at the surface or sink to
      the substrate. Some of the diets have full prey items like Mysis shrimp. Each of these
      has the potential to offer novelty when rotated. Live foods have the potential to intro-
      duce disease and parasites, and some of the diet formulations are not appropriate for
      all species. Knowledge of the species in a system as well as other aspects of filtration
      and husbandry helps to guide the choices offered to each animal.
      Feeding Behavior
      As with any enrichment, the natural behavior of the animal needs to be considered
      when selecting feeding enrichment. Different species of fish may feed by scavenging,
      foraging, grazing, or hunting.15 Learning these normal behaviors for the fish being
                                                         Environmental Enrichment for Aquatic Animals           309
cared for helps to guide an enrichment program and helps to evaluate the success of
the selected program. In addition to changing the type of food offered, other changes
can help to keep feeding novel. Some methods that have been implemented success-
fully include a rotation in feeding times and locations. Currents being added at feeding
times can simulate hunting with prekilled food.15 Sea horses have been fed with sink-
ing canisters of brine shrimp and with frozen sinking cubes of shrimp. Increased
foraging behavior was seen with both strategies.15,16 Foraging has also been encour-
aged by sinking feeders with holes. The feeders are filled with live feed that slowly
disperse from the feeder.15 Animals that prefer to hide (eels, gobis, etc) may need
to be focus fed with sinking food placed by a dropper or by feeding with tongs. Sub-
missive fish should have special attention during feedings to ensure they are getting
adequate nutrition (Fig. 2).12
   The last part of any nutritional enrichment program is monitoring. The caretaker
should watch the fish for natural behaviors, and the amount of time spent in feeding
behaviors. Body condition of animals should also be monitored regularly. If any
decreased activity or weight loss is observed, the program should be reevaluated
and, in the case of weight loss, a medical evaluation should be considered.
Housing
For aquatic animals, we are of course discussing either a bowl, aquarium, or pond.
Much is in common between the 15 gallon aquarium in a home and the 15,000 gallon
aquarium at a zoo. Both require the size to be appropriate for the species held, the
proper current, filtration, lighting, substrate, depth, and dimensions.
  Size is the first important consideration when considering what animals can
be placed in an enclosure (or what enclosure is appropriate for a certain animal to
be displayed). Size considerations include not only length and width, but depth and
volume. Dimensions in the tank (length, width, and depth) are extremely important
for some species and less important for others. Knowledge of the species is important
for these decisions and proper dimensions are necessary for the animal to be able to
display natural behaviors, and to have freedom from stress and discomfort. Several
examples are highlighted to help the reader begin to learn what considerations are
necessary in either tank design or deciding whether or not a certain species can
have proper enrichment in an existing system.
  One good example on a large scale is preparation and selection of appropriate aquar-
ium space for sharks. Many sharks are pelagic and obligate ram breathers. Pelagic
                          NutriƟonal makeup
                          Proper raƟo of protein, fat, carbohydrate and fiber
                          Quality of nutrients
                          Vitamin and mineral supplements
                                                                                Food FormulaƟon
                                                                                Live, flake, frozen or liquid
           Behavioral Aspects
                                                                                Sinking or floaƟng
           Sensory factors
                                                   Good NutriƟonal Health
           Social factors
           Environmental factors
                                                        Storage
                                                        Time
                                                        Humidity
                                                        Temperature
                                                        LighƟng
      means they are more commonly found in open water away from shore and off the bot-
      tom. Obligate ram breathers means they must continue moving forward to get adequate
      water flow across their gills for proper respiration.17 To conserve energy, these sharks
      move forward with a long gliding phase to their swimming pattern, utilizing their pectoral
      fins to generate lift and conserve energy. If the enclosure is too short, more energy is
      required for movement, and not only do the animals become exhausted, but natural
      swimming behavior is restricted. There are formulaic guidelines for determining
      dimensions, but shape of the aquarium and location of obstructions to movement
      (such as reefs) can affect the formulas and must be considered.17,18 Overhead clear-
      ance in most of these aquariums also needs to allow unobstructed movement for dorsal
      fins out of the water.18
          Depth can be important for certain species as well. Some marine fish are accustomed
      to living on reefs with steep vertical walls. One factor regarding depth can be light pene-
      tration through water. Water is a powerful filter of light. Red light penetrates a very short
      distance and the blue end of the visible light spectrum is filtered deeper. Coral depends
      on certain wavelengths of light to get energy from photosynthesis from the symbiotic
      zooxanthellae.19 The depth of the water and placement of lighting has a profound effect
      on the health of these animals.
          Depth may also be a factor in design based on the function and purpose of the aquar-
      ium with consideration for the health of the animals on display. Dimensions of touch
      tanks vary from those of tanks purely for display. A relatively shallow depth ensures
      easier interaction for visitors at a public aquarium. It also reduces surface area of skin
      from visitors when they reach into the water. This decreases toxin exposure for aquatic
      animals from hand lotions and skin bacteria. It also decreases visitor’s exposure to zoo-
      notic diseases.20 The horizontal size of display tanks needs to ensure adequate space
      for the animals on display and should give the ability for the animals to have choice in
      interaction with visitors, but allow them to distance themselves from handling as
      well.18 If it is not possible to allow choice (eg, starfish that move too slowly), then 2 tanks
      should be used in alternating fashion or an off-display holding tank should allow rotation
      of animals.20
          Proper current is the next consideration to be discussed after the size of the tank.
      Proper water flow in a system is also heavily species dependent. Betta fish have very
      large fins and naturally inhabit stagnant water in rice patties of Asia. Even a very light
      current in a system can be very stressful or even harmful for them. On the opposite
      extreme, very high flow rates are required for some systems containing river fish.
      Salmon ladders built into dams allow salmon to bypass. They need to have a strong
      current to ensure that salmon follow the proper route upstream. In the middle, coral
      require some current to carry food and nutrients to them because they are largely
      stationary in a system, but too strong of a current can damage their fragile append-
      ages.21 Proper water flow in a system also affects aeration and filtration of the water.
      Betta fish are labyrinth fish, meaning they can breathe air at the surface. They are
      also tolerant of poor water quality relative to other species, so low water flow is fine
      as long as the water changes are frequent enough. By contrast, some marine species
      have greater oxygen requirements. Salt water also has less holding capacity for oxygen.
      If the water flow is interrupted in a tropical salt water tank, some species of fish suffocate
      within hours. Koi ponds are normally designed with waterfalls or fountains, not only for
      decoration, but for aeration of the water as well. Without this aeration, water in these
      ponds can be oxygen depleted and can have increased waste gasses.22 For enrich-
      ment, some water flow can be changed with the right species of fish. Most filtration sys-
      tems have movable spouts to direct the flow of water leaving the filter and returning to
      the aquarium. There are also underwater fans or jets that attach to the inside of the
                                         Environmental Enrichment for Aquatic Animals           311
aquarium and can be located in different areas of the tank easily. It is relatively simple to
create a tidal motion using a reservoir at one end of an enclosure that gradually fills and
then rapidly empties water returning to the aquarium from the filtration system. Tidal ac-
tion is frequently used in public aquariums in the touch tanks, often filtering down
through various shallow pools of different levels. Many touch tank animals (starfish,
small crabs, etc) live in tidal pools and do well with this type of enrichment.
   The next consideration in the system is the substrate and decorations placed in the
tank. All the contents in the aquarium or pond can offer some enrichment. Substrate
can vary in color, size, and texture. They can look natural or very artificial, from sand to
colored glass beads. Although they are designed to present different decorative
effects for the observer in most cases, they are also important for the fish. They can
be important for some spawning behavior, territory marking, and nest building.9
Some examples help to illustrate the importance of ensuring the substrate is proper
for the species. Southern stingrays are accustomed to burying themselves in the
sand. They should be offered a fine, nonabrasive sand deep enough to bury them-
selves. Garden eels need a mix of fine sand and crushed coral 8 to 12 inches deep
to allow them to burrow to be free from fear and anxiety.23
   The number and type of decorations available is almost without limit. Just like
substrate, they can be very natural in material or appearance or can be very artificial.
Different options include rocks, plants (real and artificial), PVC pipes, wood, statues,
and mechanical toys. Rocks can provide a natural appearance to the environment
and add a vertical dimension to the enclosure. When arranged properly, they can
also form caves and provide hiding places for inhabitants that feel more comfortable
in caves or crevices.9 The increased surface area can provide more biological filtration
in the system (discussed further in the sections on filtration and water quality
elsewhere in this article). PVC pipes can be hidden under the rocks or holes can be
drilled into the rocks to provide cave areas. Plants can also add a vertical component
and a more natural appearance to the environment. They can provide shade to
outdoor pond fish. Wood can be a source of nutrients to some snails in aquariums.
The statues and mechanical toys like Tiki heads, skulls, “bubble volcanoes,” and
treasure chests are largely decorative, but can still provide hiding places for submis-
sive fish and novel items for exploration. Even providing these items and rotating them
randomly can change daily patterns and provide new territory.9,15
Lighting
Many advances in lighting offer great options for enrichment. Different lighting can
enhance the experiences of the observer and can enhance the well-being of the inhab-
itants or the system. Specific lighting can even be important for growth and breeding
with some species. Starting with coral, the importance of lighting spectrum can be
emphasized. Coral depend on nutrients from their zooxanthellae for growth. The
blue end of the visible light spectrum is the best for photosynthesis by these organ-
isms and is associated with the best coral growth. By contrast, red lighting has
been associated with coral bleaching events.21 Variation can also be provided by
length of day. The standard beginning photoperiod is 12 hours each of dark and light,
but this cycle rarely occurs for fish in the wild. Varying day length has been implicated
in the breeding cycles and other behaviors in many species of fish that are seasonal
breeders or that have seasonal migrations.24
   Various types of lighting are also available for aquariums. Fluorescent lighting is
common and bulbs are available with focuses of different wavelengths for different
purposes. Metal halide lighting offers more intense lighting that also seems to be
more natural in the aquarium.21 More recently, LED lighting has been introduced to
312   Corcoran
      aquarium lighting systems. The cost of these systems is now coming down to a point
      that they are becoming practical for even hobbyists to have access. Not only do LED
      systems offer better penetration into the water column, but they allow other features
      that are great for enrichment. New systems are programmable. The day length can
      be adjusted automatically throughout the year. The lights can also better simulate
      natural lighting by gradually dimming at the end of the day and reversing in the morning
      to simulate sunrise and sunset. Because LED systems are designed with multiple
      smaller lights, cloud cover and thunderstorm effects are available with some systems.
      The effects of this enrichment on fish behavior is a good subject for future research. It
      can be proposed that providing more natural lighting effects will have a positive effect
      on promoting natural behaviors in aquarium inhabitants.
      There are no unique aspects of filtration or water quality that provide novel experi-
      ences for enrichment, but discussing aspects of husbandry that promote natural
      behavior, physical health, and psychological health should include these topics with
      regard to aquatic animals. In most natural environments, there is a tremendous turn-
      over of water that keeps contaminants from accumulating. In a closed pond or aquar-
      ium, animals live in the same water in which they eat and eliminate waste. Without
      proper water quality, natural behaviors cannot occur and there is greater chance of
      disease and stress.
      Filtration
      Filtration for aquatic systems comes in 3 different types: mechanical, chemical and bio-
      logical.22,25 Most systems use a combination of at least 2 of these types of filtration. Me-
      chanical filtration uses different methods to physically remove material from the water.
      The filters may use sand, gravel, felt cloth, or other material to strain large suspended
      material from the water. Mechanical filtration contributes to the clarity of the water in
      a system, but can also help to prevent buildup of nitrogenous waste by removing large
      particles of food or other biological material from the water before decomposition. For
      these filters to work properly, they require some routine maintenance. The material may
      need to be replaced or the filter may require that the material is stirred to avoid formation
      of channels that bypass the bulk of the material.
         Chemical filtration uses chemical reactions to remove dissolved substances from
      the water.22 The most common use of chemical filtration is use of a dechlorinating
      agent to prepare water. It is important to note that most city water systems now
      contain chloramines, a more stable form of chlorine. Conventional wisdom is that
      chlorine evaporates from water in 24 hours, but this is not true of chloramines. If a
      chemical dechlorinator is not used, then toxicity from chlorine is likely to result
      from using the water. Other examples of chemical filtration include activated char-
      coal, foam fractionation, UV sterilization, and ozonation.22,25,26 Activated charcoal
      is used in fresh water and marine systems to remove ammonia, medications, or
      and some heavy metals. Foam fractionation is used primarily in marine systems.
      Very fine bubbles are formed in a closed container. The hydrophobic end of proteins
      is trapped in the bubbles and elevated to a collection cup at the top of the water col-
      umn.22,26 UV sterilization is used to irradiate the DNA and RNA of bacteria, viruses,
      algae, fungi, and protozoa. The UV light is placed in the pipes in an area of low flow
      to allow contact time.22 Ozonation is generally used in larger systems. Ozone is pro-
      duced in a closed container and exposed to the water. The ozone oxidizes organic
      compounds in the water.22,25,26
                                          Environmental Enrichment for Aquatic Animals            313
    Biological filtration is present in almost all healthy systems. Organic material in the wa-
ter breaks down quickly to ammonia. This material comes from feces, uneaten food, and
dead animals or plants. Ammonia is toxic to fish and invertebrates. The biological filter
consists of Nitrosomonas and Nitrobacter bacteria.25 They break down the ammonia
stepwise into nitrite and nitrate. This process is known as the nitrogen cycle (Fig. 3).
Each step in the process is less toxic to the inhabitants of the aquarium. Nitrates can
be removed either through periodic water changes or by conversion to nitrogen, which
leaves the water as a gas.22,25–27 To establish and maintain a biological filter, surface
area must be provided to allow growth of bacteria. Various methods are used in different
systems. Live rock and live sand can be used in plain sight on display for a natural appear-
ance. Inside the filtration system, surface area can be provided by sponges, wheels,
brushes, or plastic balls.
    There are certain aspects of filtration that are also important to note for veterinarians
and caretakers who would be involved in medical treatment. First, it is important to
remember that chemical filtration is designed to remove contaminants based on chem-
ical properties or chemical reactions. When adding medications to the water for treat-
ment of sick fish, chemical filtration in the system needs to be considered. The same
processes that remove toxins and proteins can also remove or inactivate medications.
Depending on the treatment, chemical filtration may need to be discontinued tempo-
rarily.28 This lapse can affect water quality, adding stress to animals that are already
affected by infection or another stressor. Maintaining all other aspects of husbandry
as close to normal is an important consideration for treatment. Second, biological filtra-
tion can be affected by some medical treatments. If the treatment kills the bacteria in the
biological filter, poor water quality can result and the filter may need to be re-established
after treatment. The poorer water quality will cause more stress to be added to the
illness in the fish. Finally, activated charcoal has been highly correlated with head
and lateral line erosion, a disease that may cause an animal to be presented to a veter-
inarian.29 The caretaker or practitioner should consider the effect of antibiotics or other
                                      Nitrogen Cycle
                                      Ammonia
Nitrites
                                          Nitrates
Fig. 3. The nitrogen cycle.
314   Corcoran
      medications on the bacteria of the biological filter.28 This will also add stress to the an-
      imals under treatment. Any enrichment that can reduce the stresses associated with
      treatment will help to maintain good health. Training animals for medical procedures
      is discussed elsewhere as an important method for stress reduction.
      Water Quality
      Monitoring and maintaining good water quality is among the most important aspects
      of aquatic animal care and enrichment. If water quality is not adequate, then the animal
      cannot be free from discomfort or disease and cannot exhibit normal behaviors. No
      matter the type of system, the caretaker should monitor and maintain normal
      ammonia, nitrites, nitrates, temperature, pH, and alkalinity. Other parameters that
      may need to be maintained in various systems include total hardness, salinity,
      dissolved oxygen, calcium, copper, magnesium, oxidation reduction potential,
      phosphate, and dissolved organic material, among others. The brevity of this section
      is not a reflection of the importance of water quality maintenance in an enrichment pro-
      gram; rather, the opposite is true. Entire books have been written on the subject of wa-
      ter quality. There is no way possible to have an inclusive section in this article that
      would adequately address water quality for enrichment. The reader who is unfamiliar
      with water quality should make an effort to learn as much as possible on the subject.
      Quarantine
      Newly acquired fish should always be held in strict quarantine. The author recommends
      a time period between 30 and 90 days depending on the species, water temperature,
      and source of acquisition. Quarantine also presents some unique enrichment chal-
      lenges. A normal quarantine enclosure has scant material in the aquarium or pond.
      Any substrate, live rock, or other porous surfaces are not easily disinfected between ac-
      quired animals. Excessive hiding areas make close observation of quarantined animals
      difficult. Porous materials can also interfere with prophylactic medications used in quar-
      antine. This difficulty necessitates a more artificial environment that is devoid of much of
      the normal enrichment. At the same time, it can be a period of greatly increased stress
      for the animals. Often, animals have been shipped over long distances just before quar-
      antine. Many are recently wild caught and are unaccustomed to an aquarium. During
      quarantine in many facilities, animals are subject to medications, sedation, and multiple
      examinations that add to the stress. Any allowances for reduced stress improves the
      survivability of quarantined animals.
         When possible, animals should be allowed several days to acclimate to the new sur-
      roundings before starting prophylactic treatments or performing examinations. In
                                       Environmental Enrichment for Aquatic Animals         315
many cases, feeding animals is inappropriate for the first several days of quarantine.
PVC pipe or other similar material can be placed into the quarantine tanks to provide
hiding areas for fish and reduce stress.31 Water quality should be maintained strictly.
Temperature should be maintained within the normal parameters. Many advocate
maintaining the temperature at the high end of normal to accelerate parasite life
cycles, but this needs to be balanced with stress to the animals. It is safer to use
normal temperatures and extend the time in quarantine. Stocking density should be
low in quarantine to reduce stress on the animals in the systems.31 Quarantine is
also not a safe area to mix predators with their prey items, although this is sometimes
done on display in larger systems with adequate hiding spaces for the prey animals.
Examples are large capacity reef aquariums that house sharks with other fish species
to display all animals present in the ecosystem. Lighting should reflect normal spec-
trum and timing for the species and nutrition should be high quality.
Display
For the purpose of this article, display tanks are the systems in which the animals are
maintained on a long-term or permanent basis. Display tanks can be extremely
different when looking across all possibilities. Home hobby aquariums, backyard
ponds, food farming facilities, and public educational aquariums all must be consid-
ered. Although there are many differences, some basic principles apply to all. First,
the size of the aquarium determines the species that can be displayed (or the desired
species determines the size of the enclosure needed). The species kept in the system
determines the remainder of the husbandry. Every effort should be made to keep only
species from the same regions of the world. Husbandry varies for fresh water fish from
the Amazon and Asian river, as it will between marine fish from the Pacific and the
Caribbean. The species selected (or already present in a system newly assigned)
determine the water quality parameters and water temperature. It also determines
the necessary lighting, water flow, filtration, substrate depth, and dietary needs.
Once husbandry needs have been met, further enrichment can be established.
   Again, the goal of enrichment is to encourage natural behaviors. In nature there is no
feeding schedule, but in captivity it is necessary to have some type of schedule so that
food intake can be monitored and so that excess food does not adversely affect water
quality. In nature, excess ammonia is diluted in large bodies of water. In captivity,
stocking density is much higher than in the wild, so waste is far more concentrated.
With these limitations, adjustments must be made to normal feeding, but the changes
can be mediated with an enrichment program. Just like other animals, the time spent
engaged in hunting or foraging in the wild is far more than captive animals on a feeding
schedule. It is well-documented in most other animals that the resulting time, if unoc-
cupied, leads to stereotypies and other abnormal behaviors. To deter these problems,
foraging programs are established. The same enrichment can be adjusted to captive
aquatic animals. With most aquatic animals, the actual diet can be varied. Offering
different foods can be enriching and can also help to ensure better food intake and
good nutritional balance.9 The feeding schedule and location of feeding stations
can also be varied to prevent entrainment to particular foods and schedules.9,15
Feeding near currents can stimulate hunting behavior by forcing fish to swim after
the food.15 Multiple daily feedings also helps to simulate a more natural feeding
regime. For herbivorous or omnivorous species, plants in the enclosure allow grazing
throughout the day. Finally, foraging devices can be formed by drilling holes in closed
canisters and filling with brine shrimp or other food.15
   Lighting changes can be an integral part of an enrichment program. Natural sunlight
does not turn on and off with a switch. The wavelength and intensity of light is again
316   Corcoran
      dictated by the tank design and the species on display. Enrichment can be built into
      the design by varying the lighting. Rather than an instant on and off, lighting can be
      programmed to go on and off more gradually to simulate sunrise and sunset. At the
      most simple, various lights are created for different wavelengths of light. The Actinic
      blue bulbs can be turned on earlier than the full spectrum in the morning and left on
      longer in the evening. However, with newer LED lighting systems, the lights can be
      preprogrammed to go on and off like a dimmer. These systems can also allow sea-
      sonal variations in day length. Cloud cover and storms can be simulated on some of
      the more advanced LED systems or with changing the intensity of other lights. Night
      lighting can be provided to simulate moonlight and this can also be altered to simulate
      monthly variation in intensity.9
         Furnishings need to be selected based on the species and natural behaviors. Many
      aquatic animals require hiding areas to be free from fear and distress; others need
      unobstructed access to lighting for proper nutrition. Various substrates, rock forma-
      tions, PVC piping, and other sculptures are available for home hobbyists and public
      aquariums alike. Periodic changes to furnishings can be integrated into a foraging pro-
      gram. Most aquatic animals move to new environments in the course of their normal
      interaction. Even if living on the same reef, fish move to new areas periodically in
      search of food, mates, or new shelter. Changes to furnishings can reflect seasonal
      changes of the natural environment of some species.15 Rearranging existing furnish-
      ings periodically can also encourage animals to seek new territory and explore the
      enclosure more thoroughly. Novel furnishings provide opportunities to explore and
      defend as new territory.15 Keep in mind there are some species that do not normally
      experience novel environments as often. For example, Betta fish inhabit small niche
      areas in the wild. For these species, excessive change can be stressful as well.
      Knowing as much as possible about the natural environment of the species is impor-
      tant as a foundation for development of an enrichment program.
         Water movement needs vary with species.9 From one extreme to the other, some
      fish require a very stagnant enclosure, whereas others live in tidal regions that have
      regular, drastic changes to flow. Most aquariums and ponds have external filtration.
      Placement of the inflow and outflow of the filtration establishes the basal water
      movement in the system. The number, location, and diameter of these pipes can
      change the water flow pattern in a system. In many aquariums, they are locked in place
      by designs; in others, they can be changed. In addition to the flow established by filtra-
      tion, water flow can be changed with supplemental equipment. Underwater fans can
      be attached to the inside of aquarium glass and used to direct the flow of water
      (Fig. 4). These fans can be rearranged regularly to change water flow. There are
      also systems that allow rapid water changes like what is found in a tidal pool. The
      outflow of the filtration system fills a container to a certain level, then the container
      empties rapidly, providing high flow into the system. These systems can be created
      with spring-loaded buckets that dump when filled or more elaborate systems with a
      mechanism similar to toilet flappers.
Contact with the target is bridged with a reward, usually a food item. The food item can
be attached to the target or given by a caretaker upon contact with the target. The
animal is then trained to target for varying lengths of time to get the reward.33 Once
the target training is established, then bridging that training with other procedures
can be started. Target training alone can be used to separate various animals. At
the New York Aquarium, aggressive sharks were targeted to 1 side of an enclosure
and sea turtles were targeted to the other side for treatment.34 Target training can
also be used to target animals into treatment tanks in large enclosures to decrease
capture stress.34,36
   Target training can also be used for specific procedures. Animals can be asked
to go to their targets in association with a stretcher, net, or other capture device in
proximity to the target. The capture device is placed in front of the target, deep to
the animal. As the animal is desensitized to the presence of the net, it can gradually
be brought closer until the animal accepts voluntary capture for weight checks or
transport.33,34,36 Common medical procedures that can also be associated with
target training include skin scrapes, ultrasound examination, medication adminis-
tration, phlebotomy, and handling for examination of the ventral aspect of the
animal. Similar methods are used as for capture. While the animal is targeted,
tactile stimulation is coupled with the reward. As the animal is desensitized to
the touch, it can be increased gradually until the animal accepts injections, phlebot-
omy, ultrasound probe contact, or handling for examination.36 Some degree of
training in this manner has been performed on sharks, rays, and even goldfish.
Acceptance of any of these procedures voluntarily decreases stress and risk asso-
ciated with procedures (Fig. 5).
         Owners can also be encouraged to do some target training and can do some
      training for voluntary medical procedures. Koi are extremely food motivated and
      readily respond to the appearance of their caretakers (and in personal experience
      the presence of the veterinarian). They are intelligent and willing to learn. The methods
      described herein can be used easily with koi to train them for low-stress capture and
      get them accustomed to handling. The author has been able to perform ultrasound,
      skin scrapes, injections, orogastric intubation, and even phlebotomy on some koi
      without sedation.
      Elasmobranchs
      Sharks and rays are common animals to appear in collections at public aquariums and
      are seen occasionally in private collections. They are also intelligent and readily
      trained. Not only will training for procedures and handling reduce their stress, but it
      is important to remember that many of these animals can pose a threat to the care-
      takers. Training can reduce the need for direct handling for many procedures and
      can allow easier safe restraint. Reduced stress for the animal at procedure times
      also decreases the chances that the animal shows defensive behaviors, such as biting
      or stinging.
      Cephalopods
      Octopuses are some of the most popular animals at public aquariums. Their intelli-
      gence has been recognized for some time and enrichment has been well-
      documented for the giant pacific octopus (GPO). GPOs kept in captivity without
      aggressive enrichment programs frequently display inking, irregular color patterns,
      jetting into the sides of the enclosure, and autophagy.37 They are also notorious
      escape artists. The escape attempts can be dangerous to the octopuses as well as
      inhabitants of nearby enclosures; they have been known to hunt in adjacent
      enclosures. Escape attempts were found to be far less frequent from tanks that had
      viewing windows as a form of environmental enrichment.38 The author has personal
      knowledge of a GPO intentionally obstructing the drain to overflow its enclosure on
      days when a particular caretaker was absent. Enriched octopuses also had decreased
      periods of rest and explored a greater percentage of the enclosure.37
         Multiple forms of enrichment have been documented in octopuses. One of the most
      simple and yet most effective is feeding live food.37–39 There are definite ethical
      implications to the introduction of live prey in a limited size enclosure with its predator.
                                       Environmental Enrichment for Aquatic Animals        319
Allowances for hiding areas should be used to minimize the stress for the prey item.
This also increases the time spent for the GPO exhibiting predatory behavior. A single
crab introduced into an enclosure can provide hours of enrichment for an octopus.38
Interaction with the caretakers is also a simple form of enrichment that seems to be
appreciated by the GPO and can offer several hours of enrichment.39 Unfamiliar plants
and shells can be offered, especially in sizes that allow them to be used as shelters.37
Food can be offered in a frozen cube or a puzzle box. A Mr Potato Head toy with food
hidden on the inside has been used in several aquariums.38,39 Food placed in floating
toy boats requires that the object be sunk to feed.39 Learning and exploration seems
to be both visual and tactile, so novel attempts at enrichment should take these factors
into consideration for increased chances of success.37 As a side note related to the
visual acuity of GPOs, flash photography has been shown to be very stressful and
should be forbidden to prevent fear and stress.
SUMMARY
Enrichment is not a new concept in animal care. Proper enrichment has been shown to
decrease stereotypies, increase exploration of enclosures, and decrease rest periods.
The 5 freedoms for welfare in terrestrial animals have been used frequently as a frame
of reference for enrichment programs. Utilizing these freedoms, enrichment programs
are designed to decrease stress, increase natural behaviors, and by decreasing
stress, decrease injury and disease. Aquatic animals need enrichment just as other
captive animals. There are unique challenges presented by the aquatic environments
in which they are kept, but the basic principles remain the same.
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