Thursday, February 11, 2016

What’s a pughead? A rare skeletal anomaly in fishes by Don Orth

We spend over 99% of our time teaching and learning about what is normal when it comes to the fishes.  However, there are also anomalous fishes; these are abnormal, or unusual, and deviate from what is normal. Because the occurrence of anomalies is a rare event, we don’t set out to study anomalous fish.   In normal situations, the occurrence of anomalies in freshwater fish samples is only ¼ of 1 percent or less in undisturbed communities (Berra and Au 1981).  One of these deformities is the pughead, or bulldog, a deformity that is encountered rarely in the fish world.  Warlen (1969) reported only two pugheaded specimens of Atlantic Menhaden, Brevoortia tyrannus in 1.2 million examined!  It's as rare as a four-leaf clover.   However, when we encounter these anomalies, they are mysteries to solve.  In biology the study of the abnormalities in physiological development is called teratology (from Greek, teras, meaning "monster").    
One approach to assessing the quality of our freshwaters involves sampling fishes and enumerating anomalies.  The index of biological integrity (IBI) has one component that is based on quantifying the extent of deformities, erosions, lesions, and tumors observed on a sample of fish.   As contamination by physical and chemical pollutants increases, the occurrence of deformities, erosions, lesions, and tumors typically increases.   These and other measures contribute to the nationwide assessment of stream impairment

The pughead deformity was first recorded in 1553 by French Naturalist, Pierre Belon, for Atlantic Salmon.  In 1554, Guillaume Rondelet, also described the deformity from a malformed specimen of the common carp (Gudger 1928).  Rondelet’s malformed carp head (below) very much resembles the bulldog’s  head.
Rondelet’s carp described in 1554 (Gudger 1928)
“Valenciennes (in Cuvier and Valenciennes, 1848, in the Histoire Naturelle des Poissons XXI, p. 335) found two adult pug-headed trouts in the collections of the great Paris museum…Valenciennes expresses wonder how this fish managed to obtain food since the intermaxillaries were bent backward and underneath so that they touched the tissues of the roof of the mouth. The lower jaw extended beyond the upper by its whole length; i.e., the front part of the head was abruptly rounded downward.”   Today, the pughead deformity has been documented in well over 100 fish species.
Pugheaded specimens of Brown trout (top left), Blue Catfish (top right)  Cobia (bottom left) and Striped Bass (bottom right)

Although the pugheaded specimen may appear to be damaged by some physical trauma, the deformity starts in early development.  See drawing (below) of a pughead trout hatchling by Girdwoyn (1877, cited in Gudger 1929).    An early hint that it was not an entirely genetic defect comes from observations by Quatrefages in 1888 (Gudger 1929) who described a pughead trout twin embryo, one pugheaded and one not. 

 Illustrations of pughead trout embryo (left), twenty-day-old trout embryo (middle), and twenty-two-month-old rainbow trout (right) from Girdwoyn (1877, cited by Gudger 1929)
The etiology of this deformity is seldom studied, so we don’t fully understand the degree to which it is an environmental or genetic anomaly.  Most abnormal individuals probably do not survive embryonic, larval, or juvenile stages.  In one experiment with Rainbow Trout (Oncorhynchus mykiss), Mostafa and Rezvani (2007) found the “abnormality was not significantly higher in matings with close family than normal mating, therefore it may be due to environmental factors of management problems.”

The deformed head means that brain ”deformation is practically confined to the preorbital part of the skull, about all that will be affected are the olfactory nerves and the nasal organs.”  Yung (1901) examined a brain in a 36mm trout and found the “forebrain seems to be reduced in size, the entire right side of this part from the cerebellum forward is, in keeping with the external conditions of the right side of the head, very much reduced and defective, and finally the right olfactory nerve is lacking.”  The neurological effect of the pugheaded condition has not been investigated.

During recent sampling of the Blue Catfish, Ictalurus furcatus, we encountered a pugheaded specimen (Schmitt and Orth 2015).  It was our first encounter with this malformation but we quickly learned that this rare deformity has been described in many other fishes. Most of the descriptions of the deformity are based on a single specimen (e.g., pugheaded cobia by Franks 1995).  However, we encountered 18 pugheaded Blue Catfish in the tidal Rappahannock River in eastern Virginia, a tributary of the Chesapeake Bay.   The finding was even more surprising because, despite extensive sampling in four tidal rivers, pugheaded specimens were encountered at only six sampling sites within the upper tidal zone of the Rappahannock River.   We are not able to document a specific cause for this deformity.  Rather, we hypothesized that severe and prolonged hypoxic events throughout the river when Blue Catfish eggs are developing may be responsible for the pughead condition.      

X-ray images of a normal (top) and pugheaded (bottom) Blue Catfish. Note the anomalous bone structure, characterized by a steep, bulging forehead and incomplete closure of the mouth.
The pugheaded fish looks like it swam hard into a wall; however, the condition begins in the embryo stage.   The condition may be mild or severe and likely interferes with feeding success, depending on the severity.    It should be a rare occurrence in natural populations and has been more frequently observed in aquaculture.   Chemical contaminants, hypoxia, dietary limitations or excesses, and temperature variations during larval development are reasonable postulates, as well as epigenetic control of mutations.   If you ever collect a pugheaded fish, it’s a rare occurrence.  Consider yourself lucky!

Berra, T.M., and R.-J. Au. 1981. Incidence of teratological fishes from Cedar Fork Creek, Ohio. The Ohio Journal of Science 81:225-229.
Franks, J.S. 1995.  A pugheaded Cobia (Rachycentron canadum) from the northcentral Gulf of Mexico.  Gulf Research Reports 9(2):143-145. 
Gudger, E.W. 1928. Guillaume Rondelet’s pugheaded carp. Bulletin American Museum of Natural History 28(1):102-104.
Gudger, E.W. 1929.  An adult pug-headed brown trout, Salmo fario, with notes on other pug-headed salmonids.  Bulletin American Museum of Natural History 58:531-559.
Mostafa, Y. and S. Rezvani.  2007.  Effect ff genetic and environmental factors on malformation in Rainbow Trout (Oncorhynchus mykiss). Animal and Fisheries Science 19:78-85.  
Schmitt, J.D., and D.J. Orth. 2015.  First record of pughead deformity in Blue Catfish.  Transactions of the American Fisheries Society 144:1111-1116.  
Warlen, S.M. 1969.  Additional records of pugheaded Atlantic Menhaden, Additional Records of Pugheaded Atlantic Menhaden, Brevoortia tyrannus. Chesapeake Science 10:67-68.

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