1

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

2

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).

3

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:

4

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?

5

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.

6

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

7

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

8

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

9

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).

10

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).

11

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

12

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.

13

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.

14

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

15

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.

16

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:

17

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

18

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

19

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

20

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