COME TO MOMMA ... FOREVER: MOTHER’S DAY 2013

A female  fantail sea devil beckons you to  "Come to momma....".

Many humans have a skewed view of the biological world.  Being highly visual creatures adapted to a day active lifestyle, it is somewhat natural for us to think that all organisms are also out and about during the day and at rest at night.   That is not true --- most of the terrestrial biological world is nocturnal.  It is not even true for terrestrial mammals, since 60% of all living mammals are either bats or rodents, most of which are nocturnal.

Furthermore, most of the living world does not even live on land. About 72 per cent of the Earth’s surface is covered by oceans and the largest habitat on Earth is the oceanic midwaters, the bathypelagic zone, which extends around the globe.  Extending from 3300 – 13000 ft (1000 – 4000m), it is a cold world of perpetual midnight, where sunlight never penetrates, the pressures are crushing (as great as 2 tons per square inch), oxygen levels are very low, and the temperatures are permanently near freezing.  Yet in spite of these incredible challenges some organisms have adapted to and even flourished in that environment.  But living in such an extreme environment requires extreme adaptations.

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INTRODUCING THE BLACK DEVILS

Among the most bizarre denizens of the bathypelagic zone are the deep sea anglerfishes, boney fish collectively classified in the suborder Ceratioidei. If you have never seen a deep sea angler, the following is an apt description:

“The medieval imagination, rioting in strange imps and hobgoblins, could hardly have invented anything more malevolent in appearance than the ceratioids or deep-sea anglerfishes, sometimes called black devils.”

                                                 Gregory and Conrad 1936: 193 (in Pietsch 2009)

High coefficients of weirdness .... representatives of the deep sea angler fishes.

There are 160 species in 11 families in the group, making it the most species diverse group of fish in the bathypelagic zone.  They’re not gigantic fish, large adults range from 4-10 inches (10 -25 cm) in length, although in one species adults have been captured close to 34 inches (86 cm) in length. Most are globular/spherical in shape, being little more than an enormous mouth and stomach with a tail. A few are oblong and even fewer elongated.  Most feed in midwater but a few seem to feed at or near the bottom. The common names for these families are both descriptive and fascinating; whipnose seadevils, needlebeard seadevils, fantail seadevils, dreamers, and footballfishes to name just a few

A fantail seadevil Caulpophryne pelagica.

A double spine seadevil,Bufoceratias wedli

The snaggletooth seadevil Lasiognathus amphirhamphus

The football fish Himantolophus albinares

What features allow these remarkable creatures to live in the land of perpetual midnight?   Because of the absence of light there is no photosynthesis in the bathypelagic zone and the food chain is supported by the organic material that falls from higher up in the water column. With food at a premium and prey widely spaced, these fish have to save energy whenever possible.  So rather than actively seek out prey, they simply float in the water.  To float with the least effort these fish have many adaptations to reduce their specific gravity to mach their environment, thus preventing them for rising or sinking. Among those specializations are loss of swim bladder, reduced body musculature, and a poorly ossified skeleton composed of very thin bones. Without a need to actively swim, they have lost or reduced many fins and others are reduced in size.

Radiograph of a deep sea anglerfish showing the lightly built skeleton, large mouth, and even larger stomach.

The first spine of the dorsal fin is modified and elongated, bearing a glowing organ at its tip. This organ is is structurally very complex and varies considerably between species.The light is generated by colonies of bioluminescent bacteria living inside the swollen tip. Most angler fish waves this structure back and forth like a fly fisherman (hence their name) to attract prey, although a few hold it stiff and vibrate it. 

Hemantolophus mauli, a football fish with a bifurcated lure.

In some the structure is very short, only a stub, while in other species the spine is absolutely enormous, several times the fish’s body length. 

The whipnose seadevil Gigantactis macronema with a fishing rod five time longer than its body length.

The pugnaceous dreamer Tyrannophryne pugnax, with a short rod and lure above the eyes.

One even has the glowing structure hanging from the roof of its mouth. 
 

The wonderfish Thaumatichthys axeli with the glowing lure hanging from the roof of the mouth.

Some have additional glowing structures growing from the chin area, sometimes resembling a great, luminescent beard.  

Glowing above and below, the bearded seadevil Linophryne arborifera with a bioluminescent lure and beard.

  

Adults are fish eaters and with prey far and few between these predators must make the most out of each meal. Once a prey item is close, the anglerfish quickly expands its immense mouth and gill chamber, instantly sucking the complete prey entirely into the mouth. So their mouths are enormous and the stomach can be greatly extended to accommodate large prey items.  Sometimes prey items too large.

The bearded seadevil Linophryne lucifer with a large fish visible in its expanded stomach.

Over indulgence. A 112 mm long doublespine sea devil Diceratias trilobus with a 369+ mm fish protruding from its mouth.

The sharp teeth in the mouth can fold backwards to let prey slide in more easily and erected to prevent prey from escaping.  Lacking scales, oxygen can be absorbed directly through the skin. Because water cannot be compressed very much angler fish are globular and contain large amounts of water. This enables them to resist the great pressures they are subjected to. There are many other specializations, but these should suffice to introduce the group. What is clear is that this most fascinating group is living proof of the Jurassic Park adage “Life will find a way.”

The ghostly seadevil Haplophryne mollis showing the many  ceratioid adaptations to deep sea life: thin skeleton, large mouth, reduced fins, loss of scales, globular body, small eyes.

Deep sea anglerfish are also very difficult to study.  They are wide dispersed in their environment. Few have been observed alive in their natural habitat. Most specimens have been collected in trawls sampling at great depths and because of the immense changes in temperature and pressure as the trawl comes up from depth, fish do not survive the journey. Thus they have rarely been observed alive in the lab and none have been kept permanently alive and studied long term in captivity. However, rare video of living fish filmed at depth can be viewed at http://www.youtube.com/watch?v=XUVerZsbYiw

Numerous species are known from just a few specimens. Given these difficulties, it is surprising that the first specimen was collected in 1833, when it was found washed ashore on the coast of Greenland, and described in a scientific publication in 1837.

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FOSSIL CERATIOIDS

Given that they are small, fragile, and live at mid water depth far out in the ocean basins, one might expect deep sea anglers to have no fossil record.   But they do.  It is limited and the fossils are rare, but they have been found. 

But how do these fragile, diaphanous oceanic fish even get buried in sediments to have a chance of fossilization?  Well the fossils are found in turbidites, deposits that form as a result of underwater avalanches transporting vast amounts of sediment into the deep ocean, trapping, carrying along and burying anything caught in the flow.  Earthquakes can trigger that large scale movement of sediment over the edge of the continental shelf out into the basin that become turbidite deposits.

From the coast to the ocean floor, how a turbidite deposit forms.

Given the right location and geological history, these deep sea deposits can be found at the surface.  One of those areas is the Puente Formation near Los Angeles. Two fossil ceratioid sites have been found in this formation, close to Los Angeles. Both were discovered during construction activities, one for the construction of the Metro Rail Red Line, Wilshire Boulevard/Vermont Avenue Subway Station.   These sites provide nearly all the Deep Sea Anglerfish fossils known to science. 

Several fossil species have been found.  They all belong to living genera of anglerfish and a number of them can be referred to living species (Acentrophryne sp., Oneirodes sp., Boroprhyne cf. apogon, Chaenophryne aff. melanorhabdus, Leptacanthichthys cf. gracilispinus cf. indica).  The Puente Formation is Upper Miocene in age, about 9 million years old, indicating that once well adapted to their hostile and eternally dark world, deep sea anglers have undergone little morphological evolution.

Because of their delicate skeletons the fossils are sometimes hard for the untrained eye to see clearly in the rock, so here I show just the best specimen from the Puente Fm. But it is spectacular!

Past and present: the spectacular Miocene fossil fangtooth seadevil Acentrophryne (above) and a radiograph of the skeleton of the living Acentrophryne longidens (below).

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SEXES IN THE SEDIMENTS

In reading the scientific papers describing these fossils, one notices that the authors repeatedly identify the specimens as females.  No males have ever been found. Why is that and how do paleontologists know with so much certainty that these 9 million year old fish fossils are all of females? 

Many vertebrates show sexual dimorphism ---  some kind of difference between that males and females.  That dimorphism can come in many different forms.  Sometimes it is easy to see, such as the colorful fan tail of male peacocks or different color patterns seen in many birds.  Sometimes it is behavioral, where males and females live in different areas and come together for breeding. Sometimes it is in the skeleton, the pelvis in adult male and female humans are different and those differences are related to giving birth. 

When it come to fossil vertebrates, however, things are often not so clear.  There are places where soft tissue preservation can reveal the nature of the reproductive system making sex identification fairly straight forward.  On Land of the Dead’s post for Mother’s Day 2012 we looked at exactly that kind of thing in fossil sharks from the Bear Gulch limestone (May 12, 2012: MOTHER’S DAY 2012: Celebrating Ancient Sharks, Superfoetative Viviparity, and the Earliest Record of Sibling Rivalry).  Mary Schweitzer and colleagues have been able to identify the gender of a T. rex from Montana when they discovered, in the leg bone, preserved medullary bone, a type of tissue found in present-day female birds only during the period when eggs are laid.

Theropods, the carnivorous dinosaurs, are a group that much of my research focuses on.  In a few rare instances, a large number of skeletons are preserved in a single quarry. In those cases, for any given size we can see two morphs, one that is lightly built and gracile and another that is massive and more robust.  In modern day hawks, eagles, and falcons a similar pattern of gracile/robust morphs is seen and it is the female that has the more robust build.  We can extend this from hawks to other theropods, but there is some uncertainty and we have no independent data to support it.  We cannot completely rule out that the larger morph is actually the male in these fossils.

In other cases, sexual dimorphism is evident but interpreting it is very difficult.  I, along with Drs. George Engelmann (University of Nebraska) and Brooks Britt (Brigham Young University) are currently describing new fossil reptiles belonging to a group known as drepanosaurs.  These are very peculiar beasts and their skeletal morphology presents us with many puzzles.  However, there are some truly remarkable, and wholly unexpected, differences between specimens when it comes to foot structure.  The skeletons all belong to the same species and come from the same quarry where they were found lying side by side.  We can make a strong case that what the differences we see are sexual dimorphism, but we have no idea which is male and which is female, much less why there should be such striking differences between the sexes in the foot and how this effected their biology.  It is related to behavioral differences, ecological differences, or something else?  We just don’t know.

So sexing your fossil is not always easy often not even possible.  But what is it that makes the identification of all know deep sea angler fish fossils as females so clear and irrefutable?  For the answer to that question we need to go back to the living members of the group.

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FEMME FATALES, FOSSIL AND OTHERWISE

Living in the world of eternal darkness presents many problems. As discussed above, finding prey is clearly a major challenge. Similar problems present themselves when trying to find a mate in the bathypelagic zone.

One of the striling features of deep sea angler fish is the pronounced sexual dimorphism in body size. This can be extreme, as in one species where the female is more than 60 times the length of the males and about half a million times as heavy.  The natural question is WHY??? 

Males of living deep sea anglers find their mates in various ways. In some they have enlarged olfactory organs that allow them to sense the females, by following the phermones released by the females from the lure at the end of their “fishing poles.”  Some have large eyes and may find females by seeing their glowing lures, and some have both large eyes and large olfactory organs.  

The small male of the bearded seadevil Linophryne arborifera showing the large olfactory organs (arrow) by which it is able to locate females.

After finding and approaching a females, males follow two major strategies for mating, strategies that vary by species.  In the case the male grabs onto the female with his teeth if she is nearly ready to reproduce and remains temporarily attached until spawning occurs.  After that the male releases himself and searches for another female.

But in many deep sea anglers males have evolved an amazing mechanism for reproduction. In those species the male bite the female’s skin and never lets go, undergoing a remarkable transformation.  The skin of the male grows and fuses with the skin of the female.  In some cases a projection of the female’s skin completely blocks the mouth of the male.  Their circulatory systems join and the male receives all his nutrients, already digested, from the female’s blood. Because of this, the digestive system of the male atrophies.  However, his testes enlarge to great size. In return for food and a free ride the male becomes little more than a reproductive organ, contributing sperm when breeding season comes around.  This comes at some cost to the female but those costs are offset by not having to find a mate in the vastness of the bathypelagic realm.   

Female of the needlebeard seadevil Neoceratias spinifer, with male attached near base of tail (arrow).

A female black seadevil Melanocetus johnsonii with a male attached to her underside.

A female ghostly seadevil Haplophryne mollis with two attached parasitic males.

Usually there is one male per female, but in some species there are multiple males, sometimes as many as eight, attached to a single female.  They remain alive as long as the female lives.

Drawing of a parasitic male warty seadevil Ceratias holbelli showing the expansion of tissue around the head and its fusion with the female's body.

Now there are some very interesting questions raised by this male sexual parasitism when it come to issues of how two different individuals fuse. How are hormonal and immunological issues overcome in order to prevent “tissue rejection” of the male by the female?   This has promising medical implications for humans, such as rejection of transplanted organ.  But these fish live in the ocean deeps and no one has yet been able to keep them permanently alive to study in the laboratory.  Thus the possible answer to human tissue rejection remains locked away in tiny fish living in a world of midnight and crushing pressure.

So sexing fossils of deep sea anglerfish is not as difficult as it might seem at first.  We know that in all living species of this group the males are always much smaller than females and they are not just miniature versions of females. Males are of quite different in shape (lacking a lure, having a small mouth, and missing many of the other specializations we've talked about) and frequently they are small, amorphous sacs attached to females.  Given this striking sexual dimorphism in all the living members of the group  it is clear that all the known fossils must be females. 

It's as easy as pie.  An female Chaeonphryne (above) can easily be differentiated from a male (below). Not to scale, female is ten times longer than the male. 

So when a female ceratioid says “Come to Momma” to her mate he only needs to come once and he can stay for life. It’s like the Life of Riley, only without the couch, beer, and television. And for the female every day of breeding season is Mother’s Day – her mate is always there when she needs him.

I close with the following quote from the great deep sea researcher William Beebe, who wrote eloquently of the sexual parasitism in ceratioid anglerfish thus:

“To be driven by impelling odor headlong upon a mate so gigantic, in such immense and forbidding darkness, and willfully to eat a hole in her soft side, to feel the gradually increasing transfusion of her blood through one’s veins, to lose  everything that marked one as other than a worm, to become a brainless, senseless thing that was a fish—this is sheer fiction, beyond all belief unless we have seen the proof of it”

                                                                 William Beebe 1938 (cited in Pietsch 2005a)

Dr. Theodore Pietsch, leading authority on deep sea angler fish, holding a large female. A small, parasitic male can be seen dangling from her underside.

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A COMMENT ON SOURCES

For those interested in learning more about ceratioid angler fish, the best place to start is Pietsch 2009, a remarkable and thorough summary of what is known about these fascinating creatures.  There are technical chapters on classification and evolutionary relationships that could be tough slogging for some, many other chapters covering bioluminescence, reproduction, feeding, history of discovery and study are readable. There are hundreds of illustrations in the volume, including many beautiful color photos, of both the whole fish and details of their anatomy.  The various Pietsch entries for the on-line Tree of Life project (see SOURCES below) are shorter but still quite informative.

When I was just a kid in Paterson, New Jersey there was a branch library on one of the corners of my block.  It wasn’t a gigantic library, but I could get to it without crossing a street, so I visited often.  One of the books I remember is William Beebe’s Half Mile Down.  Written in 1934, Beebe recounts his adventures exploring the ocean depths by being lowered down in his bathysphere, a steel sphere with a small glass window and just large enough for one person.  Beebe reported his observations on many deep sea organisms, but the ones that stuck with me were those of deep sea anglers, whose glowing organs would mark their passage through the dark outside his windows.  Beebe couldn’t collect specimens from the bathysphere, but he had color drawings made of what he saw.  Those of the anglerfish were fascinating and really caught my attention.  I never forgot those magical denizens of the deep and I have retained an interest in them up to the present day.  However, by the time I first saw Beebe's book I was already severely infected with the dinosaur virus and had my heart set on becoming a paleontologist.  Nothing, not even fish that looked like they came from another world, could change that trajectory.  Beebe’s book can now be downloaded freely (see SOURCES below).

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SOURCES

Beebe, W. 1934. Half Mile Down. Harcourt, Brace and Company, N.Y.: 344 pages (available freely on-line at http://archive.org/details/halfmiledown00beeb)

Beebe, W. 1938. Ceratias -- siren of the deep. Through perpetual darkenss the tiny male seeks out his mate and attaches himself to her spiny skin for life.  Bulletin of the New York Zoological Society 41: 50-53 

Carnevale, G. and Pietsch, T.W. 2009. The deep-sea anglerfish genus Acentrophryne (Teleostei, Ceratioidei, Linophrynidae) in the Miocene of California. Journal of Vertebrate Paleontology 29(2):372–378

Carnevale, G., Pietsch, T.W., Takeuchi, G.T., and Huddleston, R.W. 2008. Fossil ceratioid anglerfishes (Teleostei: Lophiiformes) from the Miocene of the Los Angeles Basin, California.  Journal of Paleontology 82(5): 996-1008.

Gregory, W.K. and Conrad, G.M. 1936. The evolution of the pediculate fishes.  American Naturalist 70(728): 193-208

Pietsch, T. W. 1976. Dimorphism, parasitism and sex: reproductive strategies among deepsea ceratioid anglerfishes. Copeia, 1976(4): 781–793.

Pietsch, T.W. 2005. Centrophrynidae. Centrophryne spinulosa. Prickly Seadevils. Version 03 November 2005 (under construction). http://tolweb.org/Centrophryne_spinulosa/22009/2005.11.03 in The Tree of Life Web Project, http://tolweb.org/

Pietsch, T.W. 2005. Diceratiidae. Doublespine Seadevils. Version 05 November 2005 (under construction). http://tolweb.org/Diceratiidae/22006/2005.11.05 in The Tree of Life Web Project, http://tolweb.org/

Pietsch, T.W. 2005. Melanocetidae. Melanocetus. Black Seadevils. Version 05 November 2005 (under construction). http://tolweb.org/Melanocetus/22003/2005.11.05 in The Tree of Life Web Project, http://tolweb.org/

Pietsch, T.W. 2005. Thaumatichthyidae. Wolftrap Seadevils. Version 06 November 2005 (under construction). http://tolweb.org/Thaumatichthyidae/22007/2005.11.06 in The Tree of Life Web Project, http://tolweb.org/

Pietsch, T.W. 2005. Oneirodidae. Dreamers. Version 05 November 2005 (under construction). http://tolweb.org/Oneirodidae/22026/2005.11.05 in The Tree of Life Web Project, http://tolweb.org/

Pietsch, T.W. 2005. Caulophrynidae. Fanfin Seadevils. Version 03 November 2005 (under construction). http://tolweb.org/Caulophrynidae/22025/2005.11.03 in The Tree of Life Web Project, http://tolweb.org/

Pietsch, T.W. 2006. Ceratiidae. Warty Seadevils. Version 17 April 2006 (under construction). http://tolweb.org/Ceratiidae/22010/2006.04.17 in The Tree of Life Web Project, http://tolweb.org/

Pietsch, T.W. 2007. Himantolophidae. Himantolophus. Footballfishes. Version 02 October 2007 (under construction). http://tolweb.org/Himantolophus/22004/2007.10.02 in The Tree of Life Web Project, http://tolweb.org/

Pietsch, T.W. 2005. Dimorphism, parasitism, and sex revisited: modes of reproduction among deep-sea ceratioid anglerfishes (Teleostei: Lophiiformes). Ichthyological Research 52: 207-236.

Pietsch, T.W. 2005b. Neoceratiidae. Neoceratias spinifer. Needlebeard Seadevils. Version 06 November 2005 (under construction). http://tolweb.org/Neoceratias_spinifer/22002/2005.11.06 in The Tree of Life Web Project, http://tolweb.org/

Pietsch, T.W. 2005c. Gigantactinidae. Whipnose Seadevils. Version 06 November 2005 (under construction). http://tolweb.org/Gigantactinidae/22011/2005.11.06 in The Tree of Life Web Project, http://tolweb.org/

Pietsch, T.W. 2007. Linophrynidae. Sinistral Seadevils. Version 02 October 2007. http://tolweb.org/Linophrynidae/22027/2007.10.02 in The Tree of Life Web Project, http://tolweb.org/

Pietsch, T.W. 2009. Oceanic Anglerfishes: Extraordinary Diversity in the Deep Sea. University of California Press, Berkeley: 557 pages.

Pietsch, T.W. and P. Kenaley,C.P. 2007. Ceratioidei. Seadevils, Devilfishes, Deep-sea Anglerfishes. Version 02 October 2007 (under construction). http://tolweb.org/Ceratioidei/22000/2007.10.02 in The Tree of Life Web Project, http://tolweb.org/

Pietsch, T.W. and Lavenberg, R.J.A 1980. A fossil ceratioid anglerfish from the Late Miocene of California, Copeia 1980(4): 906-908.

Pietsch, T.W. and Orr, J.W. 2007. Phylogenetic relationships of the deep-sea anglerfishes of the suborder Ceratioidei (Teleostei: Lophiiformes) based on morphology.  Copeia 2007(1): 1-34.

Regan, C. T. 1925. Dwarfed males parasitic on the females in oceanic angler-fishes (Pediculati, Ceratioidea). Proceedings of the Royal Society, B, 97: 386–400.

PHOTOS

Front view of fantail seadevil: http://www.itsnature.org/what-on-earth/22-sea-creatures-that-will-keep-you-dry/

Ocean zones: http://pics2.this-pic.com/image/ocean%20habitat%C2%A0

High cients of  weirdness: Pietsch and P. Kenaley 2007.

The football fish Himantolophus albinares: Pietsch 2007.

Turbidite formation: http://instruct.uwo.ca/earth-sci/200a-001/11rifts.htm

Pietsch holding female anglerfish: http://nature.ca/explore/di-ef/dsfe-3_f.cfm

All other images: Pietsch 2009.