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!

References

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.

Fluvial Fishes Laboratory Review of 2015, by Don Orth

Follow the wisdom of Calvin.

As New Year’s Eve approaches, I know it’s that time to consider New Year resolutions, but resolution making is no fun.   As soon as I write a resolution, I set myself up for failure!

Instead of making resolutions, here I review highlights of the research activities of the Fluvial Fishes Laboratory for 2015. 

It is a diverse collection of papers, including  a synthesis on the Smallmouth Bass, DNA barcoding of PDUF, first record of the pughead anomaly,  human dimension of trotlining, and the Clinch Dace in the coalfields of Virginia.

For the symposium on Black Bass Diversity, Brewer and Orth (2015) wrote a summary of the Smallmouth Bass.  The Smallmouth Bass has been widely introduced in North America and is the preferred target of millions of recreational anglers.  With future projections of climate change, the range of Smallmouth Bass will show expansions and contractions.   Competitive angling, catch and release, and emerging contaminants are prevailing challenges throughout much of its range.  A person could make a career of studying the Smallmouth Bass  -- I did!

Smallmouth Bass from New River.  Photo by Paul Bugas.

You can purchase the symposium from the American Fisheries Society  click here.  

In 2013, we started a pilot study to determine if we could identify what we had been labeling as partially digested unidentified fish (PDUF) in the diets of catfish.  Zach Moran did the first test series as an undergraduate research project and we have been using the protocol from Moran et al. (2015)  every since.    The DNA barcoding approach has allowed us to identify 27 species from PDUF, including small plain-looking minnows (Hybognathus regius) and migratory species of management concern  (Alosa sapidissima, Alosa pseudoharengus, and Alosa aestivalis).

Zach Moran, currently MS student at Arkansas Tech University.

Traditional morphological approaches to identification could never provide species level identifications once the key characteristics were digested.  The success of this investigation hinged on the prior efforts of Rob Aguilar of the Smithsonian Institution to collect and archive DNA sequences for fauna of the Chesapeake Bay.  

Since 2012, Jason Emmel and Joey Schmitt have been sampling Blue Catfish from James, Pamunkey, Mattaponi, and Rappahannock Rivers of Virginia in order to describe the spatiotemporal variation in diets.  

Jason Emmel (left) and Joey Schmitt (right) have sampled over 10,000 catfishes since 2012.

Among many unanticipated findings, we began to encounter pugheaded or bulldog specimens of Blue Catfish.    Pugheadedness  (which my autocorrect wants to call pigheadedness) is a deformation of the maxilla, premaxilla, or infraorbital bones that creates a pugheaded snout and a significant underbite.  All pugheaded specimens were captured within the tidal fresh zone (0–0.5 ppt) of the Rappahannock River; no pugheaded specimens were captured in oligohaline or mesohaline waters.  Prolonged summer hypoxia may be producing these deformities in the Rapphannock River, though more research is necessary to confirm this hypothesis.

Pugheaded specimen of the Blue Catfish

Trotlining for catfish is an old tradition, and was difficult to study because trotline fishers proved very difficult to track down.  Dickinson et al. (2015) indicate that trotline fishers fish often and harvest and eat large numbers of catfish (Channel Catfish and Flathead Catfish) from the New River.  This activity that was often driven by sustenance needs earlier in their lifetimes.  Trotlining is a declining activity at a time when other pursuits, such as kayak fishing, are increasing on the New River.  This hidden fishery and the participants are among the few river users aware of the occurrence of large catfish in the New River (photo).   

Ben Dickinson with Flathead Catfish captured with trotline on New River.

In “Isolating causal pathways between flow and fish in the regulated river hierarchy,” McManamay et al. (2015) examined how river regulation affects stream fishes through reach scale changes, not always through hydrology.    The type of dam and operation has a direct influence on sediment and temperature and was most important determinant of fish assemblage characteristics. This paper was only possible by leveraging collaborative sampling efforts conducted by the Tennessee Valley Authority. 

 

Ryan McManamay with buffalofish.

In a symposium paper, “Legacy of dams on the New River,” we described the localized effects of the dams of the New River drainage.  One of these dams, Fries Dam, is the oldest dam on the New River and is currently undergoing the FERC relicensing process.  

Map of New River near Fries.

Historic postcard photo of Fries and New River.

You may review photos describing the Fries Hydroelectric project by clicking here.   

Fries Hydroelectric project can produce 5,213 kW of energy with hydraulic capacity of 2,100 cfs.   Structures include a 41 foot high x 610 foot long rock masonry dam.  Water is diverted into a canal to the powerhouse; after flows exceed the 2,100 cfs capacity, flows are spilled over the 500 foot spillway crest.  Storage capacity is very limited due to sediment deposits above the dam.   I wrote a long, detailed letter to the FERC regarding the environmental consequences of continued operation of the Fries Hydroelectric project.

 

Google Earth photo of New River above Fries Dam. Note the mid-channel island built from the trapped river sediments.  Not present in the historic postcard photo.

In a conference paper, Michael Moore and I examined the factors constraining the persistence of the Clinch Dace (Chrosomus sp. cf.saylori) in southwest Virginia.  

Clinch Dace Chrosomus sp. cf. saylori.  Photo by Isaac Szabo

 This yet-to-be-named yellow-finned minnow maintains small, fragmented populations in this rugged landscape of the coalfields of Virginia.  In November of 2015, we flew over many of these sites with Southwings and gained a better understanding of the nature of the modifications of this landscape.   Runoff over the unweathered exposed rock elevates the ionic content of the stream water, usually far beyond the tolerance of macroinvertebrates and fish.   Here are a few photos from this flight.

So I resolve in 2016 to keep doing what I did last year.  Do research and move things along.  It seems to be working just fine. 

References

Brewer, S. K., and D. J. Orth.  2015.   Smallmouth bass Micropterus dolomieu, Lacepède, 1802.  Pages 9-26 in Tringali et al. Black Bass Diversity: Multidisciplinary Science for Conservation. Proceedings of the Symposium Black Bass Diversity: Multidisciplinary Science for Conservation, American Fisheries Society, Bethesda, Maryland.

Dickinson, B.D., D.J. Orth, and S.L. McMullin.  2015.  Characterizing the human dimensions of a hidden fishery: riverine trotline fishers.  Fisheries 40(8):386-394.

McManamay, R.A., B.K. Peoples, D.J. Orth, C.A. Dolloff, and D.C. Matthews.  2015.  

Isolating causal pathways between flow and fish in the regulated river hierarchy.  Canadian Journal of Fisheries and Aquatic Sciences 72(11):1731-1748.   DOI: 10.1139/cjfas-2015-0227

Moran, Z., D.J. Orth, J.D. Schmitt, E.M. Hallerman, and R. Aguilar.  2015.  Effectiveness of DNA barcoding for identifying piscine prey items in stomach contents of piscivorous catfishes.  Environmental Biology of Fishes  99:171-176.   DOI 10.1007/s10641-015-0448-7

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.