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An Evolutionary Look at the Anatomy and Behavior of the Galápagos Four-Eyed Blenny
Figure 1- Galápagos Four-Eyed Blenny, Dialommus fuscus, in a Tide Pool on Floreana Island, taken by
Author
By Joe Getsy
October 15th, 2012
Darwin, Evolution and Galápagos Final Research Paper
For Bill, Emily and Vincent—Thanks for a life-changing program
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Abstract: In this paper, the currently accepted phylogeny of the Galápagos Four-Eyed
Blenny, Dialommus fuscus, and other four-eyed fish was examined by using
biogeographical, ecological and morphological evidence. The methods used to test
this hypothesis included meticulous review of existing biogeographical data and
comparative morphology and ecology of four-eyed fishes and their proposed
relatives. The research determined that D. fuscus and M. macrocephalus are likely
sister species. The reason for the amphibious foraging behavior was also examined
by using Tinbergen’s questions as a rough guide. The hypothesis, which stated that
the behavior serves to reduce competition for resources and reduce the risks of
stranding and predation, was confirmed. However, D. fuscus also uses its abilities to
catch flies (Order Diptera) as a dietary supplement. The author’s personal
observation of D. fuscus supported the behavioral hypothesis as well.
Introduction: The Galápagos Four-Eyed Blenny, Dialommus fuscus, is a blennioid (suborder
Blennioidei) that is endemic to the littoral zones of the Galápagos Islands and Cocos
Island. It is about 15cm long at adulthood and feeds mostly on benthic crustaceans and
insects. D. fuscus is especially noteworthy because of its behavioral and physiological
adaptations that permit it to live amphibiously, unlike any other fish in the ecosystems it
inhabits. It is best observed in tide pools or crawling across rocks at low tide on the rocky
shores of Santa Cruz, Santiago and Floreana Islands (figure 2).
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Figure 2A/2B-- Not an Ordinary a Fish Out of Water (clubantietam.org 2012, Humann 2006)-- Why spend so much energy foraging when there’s a whole ocean of food?
Amphibious foraging is an arduous, high-risk lifestyle for a fish. Fish eyes are
adapted to seeing underwater. Some other risks that confront an amphibious fish include
desiccation, stranding and predation. Thriving in this strange niche requires numerous
adaptations to circumvent these dangers; D. fuscus’s numerous adaptations allow it to do
just this. The blenny’s namesake adaptation, four eyes, allows it to see in and out of
water. The fish’s eyes are horizontally separated by a transverse pigmented intersection
that creates four eyes, two each adapted for seeing through air and through water (Horn,
Martin and Chotkowski 1998: 45) (figure 3). With its four independently operating pupils
and lenses, its eyes can process terrestrial and submarine images concurrently, which
makes it a versatile intertidal predator. In this paper, the disputed phylogeny of the
Galápagos four-eyed blenny, will be examined and tested by examining morphological
and biogeographical evidence. The causes of the foraging behavior will be examined,
using three of pioneering ethologist Nikolaas Tinbergen’s criteria: function/adaptation
and mechanistic (phylogeny is covered by hypothesis 1) (Tinbergen 1963: 411-433).
Background:
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D. fuscus’s proportional strength and cautious behavior help it succeed as an
amphibious forager. The four-eyed blenny keeps its gills moist and moves between tide
pools to feed. The rocks of Galápagos’ beaches provide a rough, uneven surface with
many tide pools and slick surfaces. The blenny avoids desiccation by moving between
tide pools. It can skip across water, ride waves and crawl between tide pools (Neider
1999: 287). It typically spends between 10 seconds and 20 minutes out of water without
wetting its gills, although longer terrestrial periods have been recorded (Grove and
Lavenberg 1997: 526). Its muscular body allows it to propel itself across the lava rocks
where it forages; it presses its posterior on the rough surface and straightens itself to
move forward or jump.
Figure 3--The Split Eye
When it senses danger, it can also slide off the rocks where it rests in tide pools or into
the waves, or dart under rocks, which it does very quickly. The blenny usually hides from
large waves, but sometimes rides them back out to sea (Neider 2000: 760). Figure 4
shows a rocky group of tide pools typical of the kind where the blenny forages. Even if
the four-eyed blenny’s adaptations significantly reduce the risks associated with
amphibious foraging, this behavior is still risky and energy-intensive. What kinds of
selective advantages come from such a unique lifestyle?
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Figure 4--Rocky Tide Pools at Low Tide, Santa Cruz Island; photograph by Author
The Blenny’s phylogeny is currently debated, particularly its relationship with the
other four-eyed fishes of the Americas. D. fuscus, and three other fish, Anableps dowei,
Bathylychnops exilis and Mnierpes macrocephalus, raise the question of how four eyes
and amphibious behavior evolved. These could be explained by homologous or
analogous traits. These three other fish live along the west coast of Central and South
America, and could share a four-eyed ancestor with the blenny. Although there is not a
lot of genetic research regarding the relationship between the four-eyed fishes,
behavioral, biogeographical and anatomical evidence help in classifying these bizarre
fish.
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Figure 1--Proposed Phylogeny (Schwab et al 2001: 151), A. anableps and A. dowei are sister species
Figure 5 shows the currently accepted phylogenetic tree endorsed by Schwab et al
in 2001. Anableps, Dialommus/Mnierpes and Bathylychnops are classified into distinct
orders because of morphological, ecological and behavioral differences. A detailed
analysis of these fish will shed light as to whether or not their current classification is
correct.
Hypotheses:
Hypothesis 1: Phylogeny
Based on research, Dialommus and Mnierpes are the most closely related of the four-eyed
fish, and should be classified as one genus
D. fuscus is a separate species from Mnierpes/Dialommus macrocephalus
Through allopatric speciation following ancestral Dialommus macrocephalus’s
colonization, D. fuscus arose and thrived
To consider this hypothesis, biogeographic and morphological evidence must be
examined.
Hypothesis 2: Proximate and Mechanistic Explanations of Amphibious Behavior
Foraging on the beach reduces competition for food
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Amphibious foraging reduces the probability of being stranded or eaten,
especially in the relative paucity of terrestrial predators in Galápagos.
To examine this hypothesis, the selection pressures favoring amphibious foraging
behavior must be examined, and the selective advantages conferred must be
assessed.
To test this hypothesis, data on the behavior of D. fuscus and selective pressures for
its behavior must be analyzed. In terms of Tinbergen’s questions, this hypothesis tests
function (an ultimate explanation) and causation (mechanistic). Development will not be
examined as deeply because the four-eyed blenny does not raise its offspring beyond
guarding the nest (Graham 1973: 44). Phylogenetic cause of behavior is addressed by
hypothesis 1.
Procedures:
The methods used testing hypothesis 1 were based on observation and research.
Existing research and observations of each of the fish studied (Dialommus, Mnierpes,
Anableps, and Bathylychnops) were examined. Special attention was given to information
regarding the behavior, diet, habitat, and body morphology (especially in comparison to
evidently related fish and eye structure). D. fuscus was observed by the researcher in the
wild on a recent expedition to the Galápagos Archipelago.
The second hypothesis was tested through a series of observations and controlled
experiments. The first of these experiments, conducted by J. Neider in 2000, involved
detailed surveys of tide pools in a 200 m long and 25 m wide rock flat on the western
edge of Tortuga Bay, Santa Cruz Island (Neider 2000: 757-759). Neider’s research on the
blennies of this Tortuga Bay rock flat also involved the observation of 535 terrestrial
sojourns of D. fuscus. Distance from the water, time of the sojourn, time of observation
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and frequency of sojourns were recorded. Finally, five males and seven females were
preserved in formaldehyde and their gut contents examined; the type and relative amount
of prey were recorded.
Findings and Data:
Biogeographical and morphological similarities support the current hypothesis
that D. fuscus shares a more recent common ancestor with M. macrocephalus than it does
with any of the other four-eyed fishes. Figure 6 shows the current distribution of the
aforementioned candidates for a sister species to D. fuscus. Mnierpes/Dialommus,
Anableps and Bathylychnops all live on the west coast of Central/South America. Any of
them could have been swept to Galapágos by the California and then Panama or
Humboldt currents. Without the help of currents, the 1000-km journey would have been a
rather unlikely one for a small fish. Bathylychnops inhabits bathypelagic and mesopelagic
waters off the coast of Baja California and Northern Mexico, using its four telescoping
eyes to see its front, underside and top to find its prey (small crustaceans, a similar prey
as D. fuscus) and detect predators.
Anableps dowei (range shown in green in figure 6) inhabits river mouths and
estuaries from southern Mexico to Nicaragua (limited range overlap with D.
macrocephalus) of Central America. Unlike the other four-eyed fish, it tends to forage
near the surface, using its four eyes to see above and below the water so that it can see
insects and predators (Encyclopedia of Life 2012: np). Of its sister species (Anableps has
radiated into three niches of which the green area is one), A. dowei has the highest salt
tolerance, and lives in the location conducive to being swept out to the Galápagos.
Likewise, Mnierpes macrocephalus’s (range in yellow on mainland) range (assuming its
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historical range was similar) makes it a likely candidate for an ancestral species to D.
fuscus as well. Its range is large and currents could have swept an ancestral population to
the archipelago. M./D. macrocephalus occupies a similar niche to D. fuscus in that it
forages amphibiously and can stay out of water for extended periods if kept moist,
although it is slightly smaller (11 cm max) and exhibits some other minor differences
(Allen, Robertson 1994: 234).
Figure 2--Current Distribution of Four-Eyed Fishes on the Central-South American west coast, data compiled from fishbase.org, maps.iucnredlist.org and Encyclopedia of Life
Examining the anatomies and behaviors of the four-eyed fishes and their relatives
provides supports the currently accepted phylogeny (figure 5), and
provides a possible phylogenetic/evolutionary explanation for D. fuscus‘s amphibious
foraging. Fish of family Opisthoproctidae are known as barreleyes for their conspicuous
elongated eyes. The display a variety of body plans, but as deep water fish are suited for
high pressure and have proportionally small fins that would have required significant
evolution for an amphibious barreleye to colonize an archipelago that is only a few
million years old (figure 7).
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Anableps (figure 7) is slightly closer morphologically, although its eyes are
separated by a horizontal rather than a vertical divide (see appendix figures 1-3 for
comparative eye anatomy). Although A. dowei is somewhat salt tolerant, it prefers
freshwater, so an extremely salt-tolerant population would have had to
Anableps also shows some derived characteristics that it shares with other similar fish,
but not with any blenny, including ovovivipary.
Figure 7--Representatives of Families Opisthoproctidae (left) and Anablepidae (right), images Courtesy of Wikipedia and Google Images Search
M. macrocephalus displays many morphological similarities with Labrisomid
blennies (figure 8), especially D. fuscus (figure 9).
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Figure 8--Blenniidae and Labrisomidae
Figure 9—M./D. macrocephalus (top) and D. fuscus (bottom), images from (Encyclopedia of Life 2012: np)
Unlike other blennies, D. fuscus displays the derived labrisomid trait of stockiness and
large pectoral fins. In comparison to other Labrisomid, its body is more tubular and anal
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and dorsal fins are reduced in size, but sturdier than the thin fins of Blenniidae blennies.
M. macrocephalus displays these same traits. Appendix figure 2 shows the eye of D.
fuscus, which looks very similar to that of D. macrocephalus. Considering the geological
youth of the Galápagos Archipelago, a more similar species with a broad mainland range
is a great candidate for an ancestral species of a Galápagos species. Biogeographical,
morphological and behavioral evidence supports the hypothesis that Mnierpes and
Dialommus are closely related. As they are likely sister species, they could be considered
to be one genus (as several sources, including Encyclopedia of Life, advocate), but more
genetic testing will shed light on how closely related the two blennies actually are. Either
way, the behavioral similarities between these closely related species proves a
phylogenetic explanation for D. fuscus’s amphibious foraging; it descended from an
ancestral population of another amphibious fish.
Behavioral observation of D. fuscus largely confirmed the accepted hypothesis
explaining the amphibious foraging behavior of the blenny. Examining the blenny’s
location in relation to other littoral fish suggests that it strongly prefers tide pools that are
sparsely occupied by other fish. The data suggest that it is actively avoiding competition
(figure 10). The author’s personal observations confirm this notion; D. fuscus was only
observed in tide pools with few other fish and lots of rocks and crevices for hiding.
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Figure 10—Tide pool volume and number of other fish as compared to
density of D. fuscus, from Neider 2000
The blenny’s gut contents (fig.11) suggest that avoiding competition is not the
only impetus for amphibious foraging. The presence of Dipterans, the Linnaean order of
flies, in the guts of D. fuscus implies that the fish is not only using its amphibious
foraging capacity to avoid competition, but also access a new type of food that
exclusively marine blennies would not be able to eat. Thus, a taste for flies is an
adaptation that allows D. fuscus (and possibly M. macrocephalus) to maximize the return
on its risky behavior. Avoiding competition and acquiring additional calories is a
functional effect facilitated by the causal mechanisms (i.e. physical adaptations that
permit a behavioral adaptation) suited for the behavior.
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Figure 11—Food composition of D. fuscus digestive tracts, from Neider 2000
Conclusions and Future Study: In summary, current research supports the current classification of the four-
eyed fishes, especially the relatedness of Dialommus fuscus and Mnierpes
macrocephalus (figure 5). Dialommus fuscus shares many derived characteristics
with Mnierpes macrocephalus, and is likely a descendant of an ancestral population
marooned in the Galápagos. The two could be classified as the same genus (and they
are in some literature) because of this probable relationship. Schwab et al place the
species in the same tribe, which could be a compromise until more rigorous genetic
testing, possibly mtDNA analysis, is performed. Tissue strength tests could also
provide insight into the relatedness of Mnierpes and Dialommus, as well as selective
pressures of amphibious foraging (i.e. is it selecting for tough fins). Another
potential area of research could examine whether the split eye is part of a trend
towards four completely separate eyes.
Examining the foraging behavior of D. fuscus supports the hypothesis that the
behavior allows it to reduce its competition for food. The initial hypothesis did not
account for the consumption of new types of food, but the data show that D. fuscus
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will, in fact, eat flies if it can. Amphibious foraging is an even more useful adaptation
in Galápagos than on the mainland because of the relative lack of terrestrial
predators as compared to marine predators. Even though D. fuscus inherited many
of its abilities to thrive as an amphibious forager (phylogenetic explanation for
behavior in Tinbergen’s terms), it has adapted to the Galápagos and its new niche
quite well.
References:
Alonso, A., & Witoshynsky, M. (n.d.). CDF Galapagos Species Checklists - Dialommus
fuscus. CDF Galapagos Species Checklists. Retrieved September 11, 2012, from
http://checklists.datazone.darwinfoundation.org/vertebrates/pisces/dialommus-
fuscus-gilbert-1891/
Birds Gotta Fly, Fish Gotta Hop | SimBio. (n.d.). SimBio Virtual Biology Labs and
Interactive, Inquiry-driven Teaching Tools | SimBio. Retrieved September 11,
2012, from http://simbio.com/blog/post/birds-gotta-fly-fish-gotta-hop
Bridges, C. (1988). Respiratory Adaptations in Intertidal Fish. American Zoological
Society Journal, 28-79(96), 79-96.
http://icb.oxfordjournals.org/content/28/1/79.full.pdf
Doherty, P., Wassursug, R., & Lee, M. (1998). Mechanical Properties of the Tadpole Tail
Fin. The Journey of Experimental Biology, 201. Retrieved September 11, 2012,
from http://jeb.biologists.org/content/201/19/2691.full.pdf+html
Encyclopedia of Life - Animals - Plants - Pictures & Information. (n.d.). Encyclopedia of
Life - Animals - Plants - Pictures & Information. Retrieved October 15, 2012,
from http://eol.org
Fishbase, Retrieved September 11 2012 from fishbase.us
Graham, J. B. (1997). Air-breathing fishes: evolution, diversity, and adaptation. San
Diego: Academic Press.
Grove, J., & Lavenberg, R. (1997). Fishes of Galapagos. Stanford, CA: Stanford
University Press. http://tinyurl.com/9zgv3dv
Horn, M. H., Martin, K. L., & Chotkowski, M. A. (1999). Intertidal fishes: life in two
worlds. San Diego: Academic Press.
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The IUCN Red List of Threatened Species. (n.d.). The IUCN Red List of Threatened
Species. Retrieved October 15, 2012, from http://iucnredlist.org
Nieder, J. (2005). Amphibious behaviour and feeding ecology of the four-eyed blenny
(Dialommus fuscus, Labrisomidae) in the intertidal zone of the island of Santa
Cruz (Galapagos, Ecuador) . Journal of Fish Biology, 58(3), 755-767.
Nieder, Juergen. (n.d.). Welcome to ZipcodeZoo. Retrieved September 11, 2012, from
http://zipcodezoo.com/Photographers/Juergen%20Nieder.asp
Nieder, J. (2000). Ecological Observations on Dialommus fuscus (Labrisomidae), the
"Four-Eyed Blenny" of the Galápagos Islands. Pacific science, 53, 1-
3.http://tinyurl.com/9udfcrf
Owens, G., Rennison, D., Allison, T., & Taylor, J. (2012). In the four-eyed fish
(Anableps anableps), the regions of the retina exposed to aquatic and aerial light
do not express the same set of opsin genes. Biology Letters, 8(1), 86-89.
Pearcy WG, Meyer SL, Munk O (1965). A 'Four-Eyed' Fish from the Deep-Sea:
Bathylychnops exilis Cohen, 1958. Nature 207, 1260-1262.
Rockskipper (Dialommus macrocephalus) - Information on Rockskipper - Encyclopedia
of Life. (n.d.). Encyclopedia of Life - Animals - Plants - Pictures & Information.
Retrieved September 11, 2012, from http://eol.org/pages/225012/overview
Schwab, I., & al. (2001). EVOLUTIONARY ATTEMPTS AT 4 EYES IN
VERTEBRATES*. Am. Ophth. Soc., 99, 145-157.
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC1359005/pdf/11797302.pdf
Tinbergen, N. (1963). On aims and methods of Ethology. Department of Zoology,
University of Oxford, 55(4), 411-433.
Appendix:
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Appendix Figure 1—Anableps ocular close-up
Appendix Figure 2—Dialommus ocular close-up. The Mnierpes eyes look very similar
Appendix Figure 3—Bathylychnops ocular close-up
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Appendix Figure 4--M. macrocephalus ocular close-up (Graham 1997:45)
Appendix Figure 5—A tide pool with other small fish on Floreana Island. As research suggested, no four-eyed blennies were observed in crowded tide pools. Photo by author
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Appendix Figures 6 and 6—Blue footed booby resurfacing from a plunge dive and black tip reef shark. These and other formidable marine predators encourage the blenny to stay out of the open water
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Alonso, A., & Witoshynsky, M. (n.d.). CDF Galapagos Species Checklists - Dialommus fuscus. CDF Galapagos Species Checklists. Retrieved September 11, 2012, from http://checklists.datazone.darwinfoundation.org/vertebrates/pisces/dialommus-fuscus-gilbert-1891/
Juergen Nieder. (n.d.). Welcome to ZipcodeZoo. Retrieved September 11, 2012, from
http://zipcodezoo.com/Photographers/Juergen%20Nieder.asp
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