Bearded Dragon Health: Parasites and Adenovirus

Worms

Pinworms
Bearded dragons have a number of parasites and commensals, one of the most common is pinworms or Oxyurids. These nematodes are debatable parasites, since they cause no real pathology unless they super infect a captive animal that is over exposed to the eggs. Most veterinarians consider them to be pests, but mostly commensals rather than parasites. They appear as small, short, white, tapered worms approximately 5-8mm long, though rarely some may be over 10mm. These worms reside in the colon and cloaca, rarely venturing outside to be seen by the owner. They lay eggs ranging in size around 95 microns long with a roughly triangular shape and recognizably sculptured, brown shell.
The life cycle is fairly straight forward. The worms reside in the colon where they lay eggs. Eggs are passed in the feces. In the environment they mature rapidly into infectious eggs and are ingested where they hatch in the bowel and attach to the colon to mature into adult worms.

Treatment
The treatment of choice is fenbendazole, though in recent years this has proven to be largely ineffective in treating mammal nematodes due to resistance, and may be ineffective in treating reptile nematodes as well. Working with several breeders, I have noticed a significant decline in the effectiveness of fenbendazole (sold commercially as panacur). One population I have worked with has shown little or no response to fenbendazole treatment, showing that resistance has occurred in at least one population to the point of virtual immunity.
Currently there is no real treatment that is decisively effective. Ivermectins have been used with some success in reptiles, but the margin of safety is so narrow that it is too risky for most people to try. Ivermectins are another class of drug that has treated nematodes very successfully in mammals, but reptiles are extremely sensitive to it and can easily overdose and die. For that reason, it is generally considered better to live with the pinworms than to give ivermectins.

Coccidia

Two species of coccidia are known to infect bearded dragons. The first was described by Cannon in the 1960's and is named Isospora amphiboluri. The second was described by Walden in 2009 and is named Eimeria pogonae.

Isospora amphiboluri
Isospora amphiboluri has been associated with mortality and poor doing in bearded dragons and the infections can be severe. The life cycle appears to be a direct one within the intestine and it moves through the intestine as infection progresses. The prepatent period can be up to 25 days. The prepatent period is the time between infection and detectable numbers of oocysts appearing in the feces. The best way to diagnose the presence of this parasite is with modified Sheather's solution fecal floatation. The parasite infects the host by fecal oral contact and reproduces and amplifies within the host. A single oocyst can give rise to thousands of oocysts that are shed in the feces. Sporulation largely takes place in the colon or cloaca, so oocysts are infectious when first deposited.
Eimeria pogonae
Eimeria pogonae is less well understood, and may be a gall bladder infecting species, but the site of infection is as yet undetermined, though it is shed in the feces and can be detected with modifed Sheather's solution fecal floatation. Presumably the life cycle is roughly similar to I. amphiboluri and other members of the Isospora and Eimeria genera and consists of an amplification phase followed by sexual phase and the formation of new infectious oocysts. Oocysts are largely passed sporulated and infectious.
To date there has been no established disease state associated with E. pogonae, and it may actually be better classified as a commensal.

Coccidia Life Cycle
The life cycle of the coccidia in the genera Isospora and Eimeria are similar. In gut limited species that do not form tissue cysts in other tissues of the body (like Toxoplasma for example), the life cycle begins with the ingestion of the oocyst, usually from fecal oral contact.

• Ingestion
• The oocyst passes unharmed through the stomach and into the intestine.
• Excystation - bile acids and enzymes trigger the oocyst wall to split at its seams and fall away exposing the sporocysts (2 sporocysts each containing 4 sporozites in Isospora and 4 sporocysts each containing 2 sporozites in Eimeria).
  
• The sporocysts then split along tiny seams or, in those species with a Steida body, the Steida body swells and then literally pops out followed by the sub Steidal body (in those species in which a sub Steidal body is present).
• The freed sporozoites then look for host cells and penetrate the cells using organelles in their anterior end (specifically rhopteries, dense granules and micronemes). The sporozoite uses the host cell's own membrane to make a protective bubble around itself called a parasitiphorous vacuole as it pushes into the host cell's cytoplasm and takes over machinery causing the host cell to feed the parasite.
• The sporozoite then becomes a meront (sometimes called a schizont - pronounced skizont). The meront undergoes merogony (schizogony), which is asexual reproduction, and forms numerous merozoites.
• Merozoites burst from the host cell and infect more host cells. The merozoites repeat the same process as the sporozoite and a new round of merogony begins in each new infected cell, continuing the amplification phase of the infection.
• The number of rounds of merogony is species dependent, but most Isospora average around 3, though some species of Isospora and Eimeria can go through 5 or more.
• The last round of merogony results in infected cells where the merozoites differentiate into female or male and form gamonts.
• Female gamonts (macrogamonts) are a single cell. Male gamonts (microgamonts) form many cells analogous to sperm and called microgametes. These burst out of the host cell and fertilize the macrogamonts to form zygotes.
• Zygotes mature into oocysts which are released into the lumen of the gut and defecated into the environment. The oocysts of some species form new sporocysts and sporozoites (a process called sporulation) quickly and are infectious when they first are deposited. However, some species must take some time to sporulate and are not infectious for a certain period of time ranging from hours to days.

Coccidia Treatment
Treatment for coccidia has classically been sulfadimethoxine (commercially called Albon). Studies by Walden (2009) have shown that sulfadimethoxine was effective in treating coccidia, but even after 21 consecutive days of treatment, some animals were still positive. Studies conducted by Walden also evaluated the probiotic Pediococcus and oregano oil (both of which have had some success in controlling coccidia in poultry) and found that these treatments had no significant effect. Ponazuril (commercially marketed as Marquis) compounded as a 90mg/ml solution and given at 30-45mg/kg was very effective in treating coccidia.

Reference: Michael R. Walden, MS, DVM, PhD; Characterizing the Epidemiology of Isopora amphiboluri in Captive Bearded Dragons (Pogona vitticeps). PDF available at http://etd.lsu.edu/docs/available/etd-05292009-214931/
You can also check out my amazon.com reading list if you are interested in herpetoculture, herpetology or herp medicine by clicking the "Selected Herpetology References" link below.
Selected Herpetology References - New Category (1)

• Selected texts for the herpetologist, hobbyist or veterinarian.

Parasite Fecal Floatation Pictures

Oxyurid ovum with coccidia oocyst of Isospora amphiboluri. Bar = 100 microns. 200x. Used with permission.

Isospora amphiboluri oocyst. Bar = 20 microns. 600x. Used with permission.

Eimeria pogonae oocyst. Bar = 20 microns. 600x Used with permission

Adenovirus

Adenoviruses are a widespread group of viruses that infect many species including amphibians, reptiles and mammals. In recent years a poorly characterized adenovirus has been observed killing bearded dragons.
The adenovirus kills dragons by caused necrosis (death) of numerous cells, particularly the enterocytes (gut lining cells) and hepatocytes (liver cells). Recently Louisiana State University developed a PCR test to test for adenovirus in bearded dragons. The test was conducted by the Dr. Alma Roy of the diagnostic lab along with Dr. Shawn Zimmerman and Dr. Michael Walden. The standard test to date had been electron microscopy of the feces to see the viruses, and it had been assumed that the EM was sufficiently diagnostic. The study places doubt on that.
What does adnovirus do?

1. Adenovirus causes interference with cellular machinery and ultimately ruptures and kills the host cell.
2. Its cellular specificity is not understood, but it is known to use enterocytes, hepatocytes and renal cells as hosts.
3. Fatality usually results from hepatitis in severe cases or starvation in milder, more protracted cases.
4. Gross lesions are not present externally, making diagnosis difficult for the clinician.
5. Some animals have pale livers resembling glycogeniasis, lipidiasis or lipidosis grossly.
6. At least 2 outbreaks have been reported in the U.S. recently.

EM has certain pitfalls.
Threshold – is around 1,000,000 (106) particles per gram of unprocessed feces.
Time consuming – very time consuming.Preparation of samples – hours.
Grid preparation – hours.
Staining and sample to grid – minutes.
Grid examination – hours.
Expensive

PCR in a nutshell
 Disadvantages of PCR
Currently not as widely available as EM

Advantages of PCR
Quicker than EM
More sensitive than EM
Probably as specific in reality as EM
Chance for false negatives is lower than EM
Chance for false positives is higher than EM – Huh?

Chance for false positives is higher than EM. Why is that an advantage?
Production situations would rather have false positives than false negatives when introducing new stock.
False negatives introduced into a true negative population can cause severe economic consequences.
In most cases culling 100 new introductions to maintain a negative breeding population is more cost effective in the long run than having a costly outbreak in a population of several thousand.

Comparison of Results Between EM and PCR
EM
5 of 132 samples were positive for Adenovirus (3.79%).
8 of 132 samples were positive for Parvoviral like particles consistent with Dependovirus (6.06%).
PCR
117 of 132 samples were positive for Adenovirus (88.64).
So PCR is far better for detecting adenovirus in bearded dragons. So if you think you have adenovirus in your population, contact LSU.

Treatment
Unfortunately there is no treatment and positive animals should be culled from the population.

Source
Association of Reptilian & Amphibian Veterinarians - proceedings from 2007 in New Orleans.

Adenovirus EM

Electron microscopy colorized photo showing Adenovirus (red) and associated dependovirus (yellow). Copyright Dr. Michael Walden, 2009, all rights reserved.

Be Careful of Hobbyist and Birding Book Terms

Concerning Birding Sites and the Ornithology Books
You have to be careful about many of the birding books and sites. Most PhD's in ornithology know very little about chromatophore biology and they throw words around carelessly. To be fair, ornithologists are not physiologists, cell biologists or pathologists and have most of their education in behavior, ecology and taxonomy. So they can perhaps be forgiven for not really understanding the finer points of pathological conditions and the need for consistency within the scientific community that deals with these issues. Hobbyists are really bad about using terms incorrectly and that comes from much misinformation on the net and from reading books by those who are not really qualified to make a diagnosis of albinism or leucism (leukism). There are several sites with really weird definitions out there that have no pathological basis. One site that has been brought to my attention:

http://listserv.arizona.edu/cgi-bin/wa?A2=ind0011c&L=birdband&T=0&F=&S=&P=778

This one does a fairly good job at pointing out the inconsistencies in the birding literature regarding leukism.

Another problem with the bird literature is the superficial examination of the animals themselves with no real scientific scrutiny. The tendency to throw the word leucism (leukism) around is rather frightening. Any animal with a messed up patch of feathers that have gone white is called leucism by these people. Just look at the Cornell folks:

http://www.birds.cornell.edu/pfw/AboutBirdsandFeeding/Albinism_Leucism.htm

SCARY for anyone concerned with accuracy and precision, the way scientists are supposed to be.

The problem with this "bird brained" approach to the question is they are examining feathers. These are structures composed of keratin and they have no idea whether or not there is a lack of pigment, reduction of pigment or if there is an impairment of pigment transfer to the keratin. Transfer impairment would constitute a whole new pigment disorder not leukism, which has already been established as a defect involving the survival or migration from the neural crest of chromatophores. To date this has not been examined. What is more, is that many birds called leukistic are not really leukistic. They have pigment on most of their feathers, they just have patches of white. That is not really classical leukism. Pattern mutations, piebaldism, or some other disorder should be considered before the diagnosis of leukism is applied. To make a diagnosis of a disorder without understanding the basic pathogenesis is at the least VERY BAD FORM, and MALPRACTICE at worst!
Furthermore all you have to do is look at a calico cat as a good example. Due to the X chromosomes having different color genes you get two colors, right? No, you get three. One color on calicos is white. Tuxedo cats also have black and white. This is not leucism. It is a pattern mutation. The abnormal patchy distribution of white in the feathers of birds may be something similar, and this must be ruled out before they can be called leukisitc.

Regarding pigments, other sites which are not so good, I will not mention. But several of you have asked about another birding term, that really has no pathological authority. Xanthochroism is an odious term to be frank about it. It really has no real biological basis. It often is seen in psittacines and in aquarium fish. The cause is generally a lack of the melanins and other pigments that cause the yellow pigments to be all that is left, so yellow predominates. There is a problem with this term. First the term means yellow skin. Not a good term for birds, since we are talking about the feathers not the skin itself. Also it is a lack of pigments that causes the problem, not excess of yellow. To understand the pathogenesis, it is necessary to understand the proper name to give the condition. By the way, xanthism is also used for this and that is a really poor choice.
Here is a list of color abnormality definitions so you can see why this is a problematic condition to name.

• Erythrism (Erythristic) - excessive production and deposition, or distribution of red pigments (orange possibly).
  
• Anerythrism/Anerythristic - lack of production of pigments in the darker orange to red range.
• Hypoerythrism/Hypoerythristic - reduction in the amount of darker orange to red pigments so that the appearance of this color is largely absent except for traces or appears "washed out."
  
• Xanthism (Xanthic) - excessive production and deposition, or distribution of yellow pigments (orange possibly).
• Axanthism/Axanthic - lack of yellow and lighter orange pigments, depending on the point in the pigment cascade, this mutation can also cause corresponding anerythrism since erythric pigments (drosopterins) appear to come from the more yellow pteridines biochemically.
  
• Hypoxanthism/Hypoxanthic - reduction int he amount of yellow or lighter orange pigments so that the appearance of this color is only found in trace amounts or appears "washed out." This may also result in hypoerythrism since the red pigments appear to be made from the yellow pteridines.
  
• Melanism (Melanistic) - excessive producution and deposition, or distribution of melanin pigments (may be orange if pheomelanin to black if eumelanin).
• Amelanism/Amelanistic - lack of melanin production. At least three basic forms are possible, though whether all forms have been observed is questionable. 1) amelanism where the chemical cascade is defected before eumelanin and pheomelanins take separate biochemical routes, resulting in a complete lack of melanin production. 2) aeumelanism - where only eumelanin production is blocked. 3) apheomelanism where only production of pheomelanins is blocked.
  
• Hypomelanism/Hypomelanistic - condition resulting in the reduced production of melanins. At least three types are possible by restriction of production at the initial stages of melanin production, at the eumalnin production cascade or at the pheomelanin cascade.
• Iridism (Iridistic) - excessive production and deposition, or distribution of iridophore platelets (this is, as yet, only a theoretical condition).
• Aniridism/Aniridistic - (again theoretical - I have not heard this reported) lack of the formation of refractile platelets in iridophores.
• Hypoiridism/Hypoiridistic - (theoretical) reduction in the number of refractile platelets formed in iridophores.
  

So if the condition in psittacines is caused by reduced melanin for example it is really a hypomelanism or amelanism not xanthism or xanthocroism. Furthermore, many birds have blue in the feathers as a structural color, that means it is not caused by pigments but by structural design of the feather causing the reflection of blue light back toward your eye. If yellow pigment and blue structures are combined then you will perceive green. In this case if the feathers turn yellow it is a structural change in the feather and that is another defect entirely. That may be a good condition to use xanthocroism for, or perhaps another name (I am open to suggestions here).
A Word on Blue
Blue is generally a structural color and is the result of the interaction of iridophores and other chromatophores. There should be a note here that some species possess other forms of chromatophores. Leukophores (leucophores) are described in fish, but they are really iridophores that have platelets reflecting white back at the observer's eye. Being a bit of a lumper, I really do not consider leukophores a separate cell line, but some people do. I must also admit to and point out a bit of hypocrisy here, since I tend to talk about xanthophores and erythrophores, but lump iridophores and leukophores.
Among the other cells out there are some that have been called cyanophores. No they do not produce lethal cyanide. Cyan = blue. "Bluephores" then are cells that would contain blue pigments. This has thus far been unusual. Most animals do not have blue pigments, but use iridophores and other chromatophores to produce blue. However, that does not mean that cyanophores do not exist. They have been demonstrated in fish, and I strongly suspect they are present in cephalopods and would be surprised if they are not. Are they present in amphibians and reptiles? No, not so far as I can find, but that does not mean they are not present in some species and just have not been described. I do not look to find them in any known reptile species (though I would be pleased if I was surprised), but hope to find a paper one day where they have found them is some rain forest amphibian.

Chromatophores

I have had several questions of late regarding pigmentation and chromatophores.  There is a lot of information out on the misinformation super highway about chromatophores, but it is highly confusing.  Part of the reason for this is many people take information from studies done in mammals and think that can be lumped into one big pot with studies done in reptiles.  I would even argue that lumping mainstem reptile studies with studies in archosaurs might be a mistake.  The fact is they do not function in the same way, they do not go through the same development and they do not even have the same cells.  Mammals lack xanthophores (and the subclass erythrophores) and iridophores.  Mammals also lack dermal melanophores.  Mammals (some argue) do not even have melanophores, but instead have melanocytes.  The point is that the misinformation super highway (MiSH - not to confuse with MSH which is melanophore (melanocyte) stimulating hormone) is full of people that do not do the proper research and do not fully understand the subject they are writing about.  Some in the misinformation super highway's drunk lane (abbreviated 'wikipedia') do much more than confuse the issues, they actually write things that are incorrect and when it is corrected, change it back the the incorrect information (see the wikipedia article on leucism that a colleague of mine at another college tried to correct and wound up getting his stuff changed back to the incorrect information and told that he did not offer credible citations when he used research papers, peer reviewed literature and expert's text books as references).

The result is that there is a mass of confusion and it stems from the MiSH and wikipedia.  For an entry level of understanding about reptile and amphibian chromatophores you should start with the following three resources:

Reptile and amphibian variants - Bechtel, 1995 (book).

Dermal Chromatophores - Taylor and Bagnara, Am. Zoologist, 122:43-62(1972)

The Dermal Chromatophore Unit - Bagnara, Taylor and Hadley, The J of Cell Bio, 38:67-79(1968)

I will have a more thorough discussion on this topic later in the semester.

In brief, mammalian melanocytes do not appear to be the same as the melanophores in reptiles and amphibians.  Indeed, they do not appear to be the same as the chromatophores of invertebrates or fish either.  The chromatophore is a neural crest cell in its typical origin, though chromatophores not from neural crest develop in the eye.  They start out as a protochromatophore or chromatoblast.  They then differentiate into one of three, or four, types.

Chromatophore Subtypes - xanthophores, iridophores and melanophores contain all elements of all the chromatophore types.  Thus, melanophores contain pterinosomes and the iridophore plates (called reflecting platelets), but what makes them distinctly one type or another is the degree to which they contain the other structures.  Melanophores are melanophores because they contain around 99.9% melanosomes and only a small percentage of the other structures.  This is important to note, because this fact is what gave rise to the single progenitor theory for chromatophres.

Melanophores - contain mostly melanosomes and are capable of two forms of pigment production.  Eumelanin is brown to black and pheomelanin is orange to rust or rusty brown.  Melanophores, unlike melanocytes in mammals, generally do not inject their melanosomes into keratinocytes.  They are also usually able to move their melanosomes into their dendrites or into the perikaryon depending on neurohormonal stimulation.  The melanins are contained within the melanosomes.

Xanthopores - contain two major pigment bodies the pterinosomes containing pteridines and vesicles that contain fats with stored carotenoids.  Another class of organelle may exist in which the pteridines are converted to drosopterins and some people have suggested the name drosopterinosome.  However, since drosopterins are made from pteridines, this may be a bit of a splitter attitude, and really may not be valid.  But it cannot be denied that yellow pteridine rich cells occur within microns of orange or red drosopterin rich cells, so there may be something to the separation.  At any rate, xanthophores can be divided into at least two subtypes.
          Yellow xanthophores - pterinosome and pterinidine rich.  Since they are yellow to yellow orange and the term xanthophore can apply to the red xanthophores as well, there is a good argument to refer to this subtype as luteophores, but that term has yet to catch on. 
          Red xanthophores (erythrophores) - pterinosomes (drosopterinosomes) are rich in drosopterins which range from orange to red and even violet.

 Iridophores -  while possessing all the organelles of the other chromatophores, the iridophores primarily use refractile platelets formed by crystals of the uric acid based DNA components called purines.  Specifically the purines hypoxanthine, guanine and possibly adenine.  Basically theses platelets act as prisms and refract light to form certain colors and interact with different pigment bearing chromatophores to vary the colors.

The Pantherophis Question Raises Its Ugly Head and Slowinski too.

Ok, many people have been asking about the taxonomy of ratsnakes.  Notice I use the word ratsnake not rat snake. That is personal preference, it really does not matter which you use, both are generally considered correct.

First lets deal with the Russian study that said led to the internet confusion about the genus.  It was this study (and if anyone has read it they can understand that it was a poorly done study) that led people to start using the genus Pantherophis.  That is easily dispatched.  Herpetological review in 2003 rejected this (Crother et al., 2003 Herp. Rev. 34: 196-203.)  Further there has been no ruling by the International Committee for Zoological Nomenclature.  Without a ruling from that body, any taxonomic change is a taxonomic suggestion only.  Unfortunately, many people do not understand that.  You must remember that 85% of all things published are found to be wrong in scientific literature within a decade.  Do not take taxonomic suggestions seriously.  Do not jump on the bandwagon too quickly.  Many papers get published because someone is trying to get their name in the literature and they get things through by selecting journals with less rigorous review.  The last farce was Burbrink's papers that used mitochondrial DNA to try to separate subspecies that are known to interbreed and produce fertile offspring in the wild as different species and to name a color morph of Elaphe guttata after is dead friend Slowinski.  The slowinski corn snake is nothing of the kind.  Living in Louisiana I have had the opportunity to go and examine numerous snakes of this morph and I have even seen animals freely interbreeding with Elaphe guttata when placed in cages with both morphs present.  In fact the cage was about the size of a small room and had four of each kind in it.  Interbreeding occurred freely as far as I and the owner could tell.  I actually witnessed the act of breeding between the two morphs in the cage.  Therefore I doubt the validity of the species.  The resulting eggs were fertile and the offspring have gone on to breed with both morphs.  Without a reason to separate the species, the morphs must be considered to be the same species.  If they behave like a single species and there is gene flow, they must be the same species.

I could also go into the dangers of mitochondrial DNA, but that is a discussion for another time. Suffice it to say that mito DNA is bacterial in nature, freer to mutate and is a dangerous guide to deciding species. It is constructed like the DNA of a bacterium and even has bacterial type ribosomes that carry out the forming of protein from the instructions. It, like its bacterial ancestors (yes most cell biologists believe that mitochondria were bacteria at one time that became part of the eukaryotic cell) it lacks mutation correction machinery on the level of the eukaryotic nucleus and so it is more free to mutate. In nature if the nuclear DNA is similar enough, the sperm and egg of mating individuals can form fertile offspring. Thus this is a natural species. It behaves in nature like a species. The problem with all the taxonomy is that the natural species concept is ignored. Humans create delineations while nature works in a continuum. It really doesn't matter what percentage difference there is between the mitochondrial DNA of two morphs if their nuclear DNA allows them to behave like a single species in the wild.

Bottom Line:

I do not accept the slowinski corn snake nor the genus Pantherophis as valid.  There is simply no reason to.

Turtles, Tortoises and Terrapins

Another question that seems to be giving people some trouble is the difference among the terms turtle, tortoise and terrapin.  Ok, no one group will be pleased with me taking this on, but at least some will agree with my definitions.

1) There is no set definitions.  Its true.  Take terrapin.
Oxford's Compact Dictionary says:   • noun a small freshwater turtle.

Not very specific is it?  Also many herpetologists and some herp texts will say that terrapins live in brackish water.

Turtle?
Oxford says noun 1 a marine or freshwater reptile with a bony or leathery shell and flippers or webbed toes.
Other dictionaries give other definitions like:
Any of various aquatic or terrestrial reptiles of the order Testudines (or Chelonia), having horny toothless jaws and a bony or leathery shell into which the head, limbs, and tail can be withdrawn in most species.

Ok, one says they are aquatic one says they are either aquatic or terrestrial.

Tortoise?
The only one anyone seems to have any form of agreement on is tortoise.
: any of a family (Testudinidae) of terrestrial turtles; broadly : turtle 
:noun a slow-moving land reptile with a scaly or leathery domed shell into which it can retract its head and legs.

Wait, that is not really specific.  Well most agree that tortoises are terrestrial.

The fact is that nothing is really settled and there are regional uses of the words.

To make things even more confusing, the scientifically accepted common name of the eastern box turtle is eastern box turtle and the scientific taxonomic name is Terapene carolina.  So here is an example of an animal that is both a terrapin and a turtle!  What is more is that it is terrestrial!

2) Take a definition and run with it.  That is the best thing you can do.  Most of the herpetologists I deal with use the following set of definitions, and I use this set too because it gives us a standard that we can use.

Turtle:  any testudine, a broad term roughly synonomous with Testudines and including aquatic and terrestrial species.

Tortoise:  any terrestrial testudine (turtle) that generally has elephantine appendages and a high domed shell (though the shell has its exceptions).  The most commonly accepted genera for tortoise standards are Geochelone and Testudo.

Terrapin:  any turtle on the table or in the kitchen.  The term terrapin came from the Algonquin Indian language and meant edible turtle.  Thus, it is a culinary term not really a scientific term, and should remain so.  Only when it is part of the accepted name should it be used such as Diamondback Terrapin, but it should not be used to refer to a group of animals as a way of classification, unless you are a chef.

Leukism (Leucism)

Leukism (Leucism)

Pronunciation Problems to Ponder

Many questions have been asked of me as a herpetologist and veterinarian. One of these is the nature of leucism. First of all, it is NOT pronounced "loo-si-zm" saying that immediately identifies a person as poorly educated in scientific and medical terminology. In Classical Latin the C is always pronounced like K - the so called hard C sound. You do not call a neoplasm of blood cells "loo-see-mee-ah" it is pronounced "loo-kee-mee-ah." The rule is the same for the prefix leuc- or leuk- across the board. White blood cells are pronounced "loo- ko- site" not "loose- o- site" (which incidentally, is spelled leukocyte or leucocyte with the k form being more common, but both correct). It is "loo- ko-" in the words leucoencephalomalacia and all other words with the prefix. Arrogant as it sounds, in many medical circles the mispronunciation of basic words like that makes people think of you as poorly educated and without a firm grasp of scientific or medical language. In fact, one colleague of mine once heard another doctor say "loo-sis-tic" and said "did you hear that? Where did he get his doctorate? From an online college staffed by trailer trash?" Ok, I agree that is harsh, but similar (though more tactfully expressed sentiments ) are frequently found in the halls of academia. So mispronouncing words can make people dismiss you as a rube, so make an effort not to do it.

Where does this come from? Leuc- is the Latin form of the Greek Leukos. Thus, technically any work that is spelled with the leuc- prefix can be spelled with the Greek prefix instead and spelled leuk-. An example is the word leukocyte. The Greek is used, but it is acceptable (though more rare) to spell it with the Latin to form leucocyte. In the case of leucism the opposite has become true. The Latin form has become more widespread, but the Greek is equally valid. Thus, leukism is correct. In fact, I have increasingly begun to spell it with the Greek spelling because of the pronunciation issue.

Unfortunately, most people that pronounce it "loo-si-zm" are hobbyists that are poorly trained in medical terminology, if they are trained at all. Most know nothing about science beyond their high school biology and chemistry classes. It is very difficult to correct people that have formed an entire community which is equally badly educated. You fall into a form of peer pressure to be wrong. If you pronounce a word correctly when everybody else is pronouncing it wrong you are looked at as a jerk or a wierdo. Veterinarians and some herpetologists then adopt the incorrect pronunciation so they will not offend their clients. This is what scientists and medical professionals have to combat. Peer ignorance pressure is difficult to overcome. I can remember speaking to a group of hobbyists not long ago and someone asked me a question about leukism. I corrected their pronounciation very politely, but you should have seen the looks from the whole room. I said, "I'm sorry, do you mean leukism?" The person looked a little puzzled. I continued by saying "the condition is called leukism, it comes from the Greek leukos meaning white." The whole room smiled and looked rather odd. I asked several people afterward why they looked odd. They laughed and said "everybody says 'leusism'." When I pointed out that was not correct, they replied "maybe, but if you say it like you say it, people will think you are wierd."

For that reason (as I mentioned before) I still tend to write using the more common spelling with a C, but I have increasingly begun to spell it with a k when dealing with hobbyists.


Concepts to Consider
There is a great deal of bad information out there (hence the new term "wikipedian information"). If you have not run across that term, you will eventually. One of the greatest sources of misinformation is wikipedia. I have read the article on leucism there and there is a great deal of misunderstanding. One of the things that is not understood is the fact that the words leucism (or leukism) and albinism are essentially the same in their roots. They both mean white. The medical field is what delineated a difference between them. Those not in the medical field rarely use the distinction correctly. Just because something looks white does not mean it is either leukistic or albino. There are other genetic mutations out there that cause feathers or hair to be white which have to do with deposition of melanin or other pigments (carotenoids in many avian species for example) that have nothing to do with leukism or albinism. Many PhD's (and I am one as well as a DVM) have a very poor concept of what constitutes these conditions. So I will break them down in the most basic forms.

The first thing we must remember is the definitions are artificial. The term albino and leucistic actually literally mean the same thing - white. The artificial division between them began in the veterinary and herpetological communities, and rather recently too. In fact the word leucism has not made it (as of this writing) into most dictionaries. Among those that study chromatophore biology and pigment mutations there are a set of definitions for these words that are accepted as the standard.

1) ALBINISM- genetic mutations that alter the pigment cells of the skin and other tissues in such a way that the pigments themselves are not formed in their final, normal biological form. NOTE I said skin and other tissues. If the skin and rest of the body is not devoid of pigment, but the hair or feathers are white, that does not equate to albino. Also albinism is a derangement of pigment formation, not deposition. There are numerous forms of albinism. In humans, there are two pigments. Eumelanin is brown to black and pheomelanin is rusty or even orange or red. They travel along a similar cascade when being formed but differ in the amount of sulfur in the final melanin compound. Any disruption along the cascade can cause a form of albinism. Some albinos have red hair because they have a gene that is faulty for the formation of eumelanin, so they are really only eumelanistic albinos. Other pigments found in reptiles can also have faulty genes. The pteridines and drosopterins in the other cells (xanthophors and a subset of xanthophores called erythrophores) can cause other forms of albinism. Currently the iridophores (which use crystals and refraction to cause color instead of pigment) are not really known to be faulty in the same way since there are not pigments, so iridophoric albinism is something that simply does not occur.

2)LEUKISM (LEUCISM)- medically defined this is a defect in the skin, not the pigment cells. There are other derangements of pigment that can cause a whitening effect, but they are not classical leukism. Classical leukism is caused by a faulty gene, or set of genes, that causes the skin to be unable to support pigment cells. Experiments have been done that illustrate this. In one set of experiments normal pigment cells from a normal animal were placed in albino skin and the cells were normal and produced pigment. This demonstrated that the albino defect was in the pigment cells of the albino but not in the skin itself. The same experiment done in leukistic skin caused the normal pigment cells to die. Some have claimed that the reason eyes are pigmented in leukistic animals is because the pigment in the eye comes from another origin (the non-neural crest theory). This is really not the case. In fact some (unfortunately as yet unpublished research that really needs to get published) experiments were done transplanting RPE eye pigment cells into the skin and they died. Conclusion? Well nothing. The eye pigment cells can't survive out of the eye is all that proved. So melanophores from the iris were transplanted and they died in leukistic skin but survived in albino skin. Conclusion? The defect has to do with the skin, not the origin of the pigment cells. Further evidence of this can be found in numerous species that have melanin or other pigments present in other tissues such as the peritoneum but are typical of leukistic animals on the outside when alive.
However, some leukistic animals are also leukistic internally. What does this mean? At present it is unknown. It might reflect a subtype of leukism where there is agenesis, dysgenesis or complete necrosis embryologically of the chromatophores. This could represent another branch on the leukism scheme and might indicate a disorder we might call Complete Leukism. Where forms just limited to the skin might be termed Cutaneous Leukism. One thing is clear, the definition of leukism is only semi set. There is room for other forms, but it should be understood that there must be a standard definition defined in pathological terms.

So are there other forms of leukism? Possibly, but one must not confuse leukism with dysregulation of dysfunction of chromatophores. For example, if the chormatophore cannot produce pigments, but is otherwise functional, that is albinism. However, what about a mutation in a receptor that causes the pigment cell to be unable to receive signals (a MSH receptor for example) to produce pigment? That situation is more closely related to albinism since the pigment cells are present but not functioning, though they are dysfunctional from a different cause. Thus it is probably better call the condition something else in order to eliminate confusion. I personally refer to these potential disorders as receptor mediated chromatophoropathies (or chromatopathy) or RMC's. I first coined that term back in 2003, but have had no real case where this could be proven. Since many of the immunohistochemical markers for mammal receptors do not work in reptiles and leucistic or RMC mammals are much harder to come by, I have not been able to publish the term in the mainstream literature. But published or not, it is useful for this discussion. We can separate some of the confusion like this:

1. Classic leukism is due to chromatophore necrosis, apoptosis, dysgenesis or agenesis - and is the the absence of recognizable chromatophore cells on histopathology.
2. Receptor Mediated Chromatophoropathy (RMC) is a white state due to chromatophores not receiving signals or are receiving only low level signals to produce pigment due to a mutation in some receptor, signaling pathway or a defect in the production of melanophore stimulating hormone (MSH), but chromatophores are present in the skin on histopathology.
3. Albinism is a defect of pigment production within the chromatophores without loss of chromatophores. Chromatophores are present in the skin, but are not able to produce pigment or fully formed pigment.

3)Any white animals with pigmented eyes are leukistic? NO. Particularly in those animals where their color or percieved color comes from keratin structures like hair or feathers. There are other mutations out there where the pigment cells are working but the (in the case of mammals for example) melanocytes are prevented from injecting their melanosomes into hair shafts. This causes white coats, but pigmented skin. Some white haired horses are an example of this. They may have black skin, but white hair. They are not leukistic. Other animals have this kind of situation too and it can arise as a mutation in a population. Birds may also have a condition like this where they are really normal as far a pigment production, but not in terms of deposition in the feathers.

4)Animals with patterns are leukistic, right? NO. Leukistic animals should be all white. There was a picture of a giraffe circulating about the internet a few years ago that was black and white. No brown. People started calling it leukistic. NO. It had black, so it was not leucistic. It may have had a pheomelanin defect or other mutation, but it was definitely not leukistic. On the wikipedia website under leucism there is (as of this writing) even a picture of several avians with black feathers but white feathers also. That is NOT leukism. Pattern mutations are something separate as is piebaldism. Piebaldism was believed to be a related condition to leukism, but it is often a progressive condition over time in animals, though may be static. Animals that are born with a pattern that is maintained over the course of their life may not be piebald, that is often something else, like mosaicism or a pattern mutation it depends on the nature of the color pattern. Too often I have had someone show me an animal with a clear case of pattern mutation where the normally white bands (kingsnakes are a good example) are wider than usual and less neat, and they call it piebald. It is not so.
Typical progressive piebald animals start out normal then loose patches of pigment over time until they reach or get near maturity when it often stops progressing, though some can progress to complete loss of pigment. However, some species have static piebaldism too, but whatever the type, piebaldism is random, not patterned. Thus animals with white patches that form a symmetrical pattern are not piebald, but are suffering from a pattern mutation. One must also be careful not to throw the word around carelessly. A spotted horse is not piebald just because it is spotted. Horses are not piebald just because they have white. If the skin under the white spots is also devoid of pigment, then that may be considered piebald. But caution must be used with piebald too.
What exactly consititues a piebald? Piebald is where normal pigmented skin and structures (hair, feathers) are randomly distributed around the body with non-pigmented skin and structures. If the skin under the coat is normal, it is not piebald. Some argue that there is also another condition to piebald and that it must be an abnormal condition.
Under this definition of abnormal, paint horses are not piebald since their color is normal for the breed. Calico cats are not piebald, though they have a random arrangement of color. I personally do not accept this definition. I do, however, accept the prerequisite that the distribution of piebaldness is random.
A bi-colored crow or grackle that is symmetrical and has a distinct pattern is not piebald or leukistic, but has a pattern mutation. White pigeons with black speckles are not piebald or leukistic, they have a speckled pattern mutation. The list goes on. If you want to see misidentified pictures just look at any number of websites - they will often have a spotted pigeon and call it leukistic or piebald.
I must also bring a point of standardization here. A sparrow with a white patch around its head is more in keeping with piebaldness than leukism. Leukism is complete lack of pigment over the body. Not patches. Not blotches. Not stripes. Random patches of depigmentation are due to a pathologic disease resulting in depigmentation or due to something like piebaldism. The purity of the term leukism must be preserved for the sake of standardization. The way the current use is (especially in birding circles) if you say something is leukistic, you do not know if it is piebald, hypomelanistic, has autoimmune depigmentation, been burnt and has a depigmented white area, has a birth mark causing the hair or feathers to be white, or is completely white with pigmented eyes. UNACCEPTABLE, ASININE AND INTOLERABLE. Especially the scientific community should know better that allow this kind of confusion.

5) For lack of a better term... PSEUDOLEUKISM - I choose to coin the term pseudoleukism to identify the condition of false leukism seen in those animals (birds particularly) where pigment is dietary. Picture a flamingo which is stark white and has pigmented eyes. It is leukistic! Wrong! In point of fact this condition is common in avians. Many avian species do not deposit the classical pigments in their feathers. Many dispose of excess pigment from their diet by excreting it into the feathers as they are forming. Carotenoids are a common one. You would be surprised how many people have told me they have seen leukistic flamingos at the zoo. If flamingos, cocks of the rock or other species are not provided carotenoids in their diet, they go white. They are not leukistic or albino.

I added the following because of some questions generated by some of you. You e-mailed me some places to visit that were birding sites where they claim that washed out birds with low levels of pigment are leukistic. I hope this explanation helps.

6)HYPOMELANISM - another source of confusion out there is the really bad tendency of the literature particularly the non-peer reviewed literature of mammal and bird color morphs to call those with lower than normal levels of pigment (not absence) leukistic. The problem with that is that there is a wholly different pathogenesis going on there. I have had the opportunity to examine some of these birds at necropsy and I examined their skin and feathers. The ones I have examined were very similar to hypomelanistic reptiles. The melanophores are present but have a reduced level of melanin production. The exact pathogenesis of hypomelanism is not worked out but it is known that in some species it is a Mendelian recessive gene. It is not classical leukism, nor should it be referred to as leukism (leucism).

So there is a brief run down on leukism (leucism). Be careful what you read out there. Some explanation on leukism can be found in the book "Reptile and Amphibian Variants" by H. Bernard Bechtel. He talks about the skin micro-environment defect briefly and the transplant experiments. Keep your questions coming and I will try to answer. I hope my students have found my new blog. I will be e-mailing you all again to update you since it is now up. I will try to post my old posts eventually, but necropsy has been heavy lately and I am swamped with cases.