Why Does the Male Goby Sing? By Don Orth

Do you now why the male goby sings?

We sometimes encounter two very similar fish species in similar places. When the two species are difficult for the novice to differentiate, we further wonder “How are the species reproductively isolated?”  Ernst Mayr, a leading evolutionary biologist of the 20^th century, classified reproductive isolating mechanisms into pre-zygotic (act before fertilization) and post-zygotic (act after fertilization).  In the case of sympatric species, behavioral isolation may involve distinctive behaviors designed to increase contact between breeding individuals of the same species. Post-zygotic mechanism are less efficient for reproductive isolation.  Although, we don’t often observe these isolating behaviors, there must be some subtle cues present during breeding.   Fish use pheromones (smell), vision, and sound for species recognition and reproductive isolation. Yes, fish make sounds that travel well underwater. We’ve known this for a long time (Myrberg et al. 1965; Gerald 1971).  Listen to a few fish making sounds here.

Reported maximum detection or propagation distances of mating sounds for (a) goby Gobiidae, (b) Oyster Toadfish Opsanus tau, (c) Bicolor Damselfish Stegastes partitus, and (d) Black Drum Pogonias cromis (Amorim et al. 2015).

Recent studies confirm that many fish species communicate via sound during courtship. Typically these are low-frequency sounds produced by males when close to females, while other fish make long-distance sounds to advertise their location. Black Drum Pogonias cromis can communicate up to 30–100 m (Amorim et al. 2015).  Goby males emit sounds from their nests to attract mates (Malavasi et al. 2008). It may not sound like singing to humans. But the male fish sings in order to attract a mate. There is enough information in the sound signals that the female can assess size and condition of potential mates.  In a recent paper, Eva-Lotta Blom and coauthors studied two species of gobies (Gobiidae) to examine visual and auditory cues during courtship. Two species, Common Goby Pomatoschistus microps and the Sand Goby Pomatoschistus minutus, are members of the species-rich family Gobiidae.  Gobies are small, benthic fishes with modified pectoral fins fused together, two dorsal fins, and often distinctive color patterns. Many are popular aquarium specimens favored for their colorful patterns or behaviors. See gallery of gobies. 

The Common Goby and the Sand Goby have sympatric distributions. During breeding they are found in close proximity, often competing over the same nest resources. To study the role of vision and sound in reproductive isolation, Blom and coauthors simultaneously recorded sounds with a hydrophone and visuals with a camcorder of breeding individuals under controlled lab conditions. What they learned was that females like males that sing.  In addition, there were visual cues that differed between species so that a female Common Goby would not be fooled by the behaviors of a male Sand Goby. 

 Common Goby (left, by Michel Barrabes) and Sand Goby (right, by Mazzun Tar-Ramel)

Differences in courtship behaviors and cues also help explain why the two morphologically and ecologically similar species select different habitats for breeding.  The courtship sound of the male Common Goby has shorter duration than the one of the Sand Goby.   Male Common Goby swim faster than male Sand Goby during courtship displays.  Finally, only the female Sand Goby display black eyes during courtship.   Nests of Common Gobies are more prevalent in shallow, soft bottom areas whereas Sand Goby nests use Mya clams in deeper, sandy beaches. The habitat differences influence sound transmission.

Oscillograms of representative sounds illustrate the distinctness of sounds of (A) male Common Goby and (B) male Sand Goby.  (Blom et al. 2016)

During breeding, visual cues are typically expressed by males as breeding coloration.  In the Sand Goby, the female display of black eyes acts as a declaration of intent that the female is ready to mate. Female Sand Gobies are able to change eye coloration, sometimes gradually, other times quickly, even within seconds.   The black eyes are not conspicuous in males.  In experimental aquaria, Olsson et al. (2017) observed that occurrence of female displaying dark eyes are more likely in those females close to spawning readiness, as measured by body roundness.

Bar chart illustrating the relationship between female roundness and frequency of dark eyes (black line). Frequency of dark eyes are illustrated in dark grey bars.   (Olsson et al. 2017).

As the studies of gobies illustrate, females prefer males that sing and can distinguish sounds for closely related species in order to isolate species reproductively.  The study raises questions about how males learn to sing and whether and how noise from human activities affect signals during breeding.   But now  you know why the male goby sings.

References

Amorin, M.C.P., R.O. Vasconcelos, and P.J. Fonsesa. 2015.  Pages 1-33 in F. Ladich, editor.  Sound Communication in Fishes.  Springer.

Blom,E-L., I. Mück, K. Heubel and O. Svensson. 2016. Courtship sound and associated behaviours of two sympatric marine Gobiidae species – Pomatoschistus microps and Pomatoschistus minutus. Environmental Biology of Fish 99: 999–1007.

Gerald, JW.1971. Sound production during courtship in six species of sunfish (Centrarchidae). Evolution 25:75–87.

Malavasi S, S. Collatuzzo, and P. Torricelli. 2008. Interspecific variation of acoustic signals in Mediterranean gobies (Perciformes, Gobiidae): comparative analysis and evolutionary outlook. Biological Journal of the Linnean Society 93:763–778.

Myrberg AA Jr, E. Kramer E, and P. Heinecke. 1965. Sound production by cichlid fishes. Science 149:555–558.

Olsson, K.H., S. Johansson, E-L. Blom, K. Lindström, O. Svensson, H. Nilsson Sköld and C. Kvarnemo. 2017. Dark eyes in female sand gobies indicate readiness to spawn. PLoS One 12: e0177714  http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0177714

Sound, Sediment, and Fishin’ with Minnows: Whitetail Shiner Cyprinella galactura. by Don Orth

No one is sure how or exactly when it happened; but the consequences were irreversible.  My guess is that some fishermen brought live bait caught near their homes (perhaps in Smyth county) to fish in the New River.  At the end of the fishing day, the bait bucket was emptied into the New River to feed the local minnow eaters.  This bait minnow dumping happened more than one time.  In the springtime the dumped minnows that survived the predator gauntlet would need to locate suitable mates in order to found a new population.  The surviving minnows realized the benefits of shoaling behavior and visual and auditory cues to identify the right individuals to mate with.  From these bait minnow introductions, a new population of minnows was founded in the New River.

The Whitetail Shiner Cyprinella galactura (Cope 1868) is now a common minnow in the New River drainage.  However, this species did not appear in any fish collections from the New River during the first half of the 20^th century (Jenkins and Burkhead 1994).  The only other Cyprinella native to the New River is the Spotfin Shiner Cyprinella spiloptera.  The New River has relatively few native fish for a river of its size, but it does support several endemic fishes. During the last ice age, the New River was an upland refugia for fishes as the glaciers moved southward.  After the glaciers retreated, fishes colonized the New River drainage from uplands and lowlands, but dispersal from lowlands was inhibited by Kanawha Falls.   Consequently, many large river fishes such as the shads Dorosoma, carpsuckers Carpiodes, buffalofishes Ictiobus, and redhorses Moxostoma, never naturally colonized the New drainage.   However, many non-native fishes, including the Whitetail Shiner, are now established in the New River drainage (Buckwalter 2016). 

Whitetail Shiner  (top is live specimen from New River, bottom is same specimen after fixing in formalin) photo by DJ Orth

The Whitetail Shiner is one of 32 species of Cyprinella, the second largest North American genus of Cyprinidae after the Notropis, or true shiners.  The Whitetail Shiner is easily distinguishable by the pale white spots at the base of the caudal fin.  Otherwise it resembles the Satinfin C. analostana, Spotfin C. spiloptera, and Steelcolor C. whipplei shiners. Like these shiners, it has a terminal to slightly subterminal mouth and a terete body, only slightly compressed.  The membranes of the last 3-5 dorsal fin rays are pigmented. The name Cyprinella means little carp-like fish and galactura refers to the pale “white” spots on the caudal fin.  All species of Cyprinella are recognized by the large, vertically oriented, diamond-shaped scales, each outlined with black pigment. The head of breeding males is covered with many tubercles.  Breeding specimens are more colorful with red or orange coloration on snout and fins.   For other images of the Whitetail Shiner, click here for photo by Uland Thomas, here for photo by Lance Merry, or here for photo of breeding male by Isaac Szabo.  These photos provide examples of different specimens with different coloration of snout and fins.  

All species of Cyprinella are crevice spawners.  Males establish dominance hierarchies around crevice nesting territories.  Females deposit eggs inside small crevices of rocks and submerged logs or roots and males fertilize the eggs and defend the young until they embryos hatch. In this photo,  Lance Merry captured several males in breeding coloration during agonistic encounters.

   
Whitetail Shiner occurs in highland streams both east (Ozark Plateau and Ouachita mountains) and west  (Tennessee and Cumberland drainages) of the former Mississippi Embayment, a relict feature from a warmer geologic period.  In these clear and cool streams the Whitetail Shiner occupies deep pools near riffles, often associated with large boulders and rocky banks.   Whitetail Shiners adapt well to life in aquaria and will readily feed on flake fish food; consequently, this species has been propagated by Conservation Fisheries, Inc., for use as a freshwater mussel host.  

The Whitetail Shiner appears to be able to persist in streams that are altered by excessive sedimentation (Sutherland 2007), whereas other crevice-spawning minnows appear more sensitive to stream sedimentation (Jelks and Burkhead 2001).   Sediment movement and deposition is a pervasive issue in flowing waters and fine sediment additions result in higher suspended loads after runoff and higher sediment deposition on streambeds.  Because of the dynamic nature, the influence on fine sediments on crevice-spawning minnows has seldom been investigated.   The experimental apparatus invented by Andrew Sutherland (2007) consisted of slow moving motor-driven paddles in experimental tanks to keep the fine (less than 45-μm) sediments suspended.   Experiments on the effects of suspended solids on Whitetail Shiners demonstrated a reduction in larvae produced as suspended solids increased (Sutherland 2007).  Additional experiments on Whitetail Shiners demonstrated an additional deleterious effect on suspended sediments on gill health and growth rates (Sutherland et al. 2007).  These findings suggest that gill damage and subsequent impairment of respiratory function may explain the reduced growth.  The mainstem New River, where the new population flourished, has a reduced sediment load due to Claytor Dam, which serves as an effective sediment trap. 

Claytor Lake and Dam  (dam located in upper right area of photo) Photo by Rui M.

How would those very first Whitetail Shiners manage to find appropriate mates in this large river?  The answer lies in the non-random and innate behaviors of these fishes.  They are not random wanderers in the river; rather, they have distinct habitat preferences, shoaling tendencies, specific spawning requirements, and acoustic signals.   Whitetail Shiners also communicate with each other with species-specific calls in addition to visual signals.  Catherine Phillips and Carole Johnston of the Fish Biodiversity Lab at Auburn University observed behaviors of Whitetail Shiners associated with different behaviors in lab experiments. They discovered that males make low frequency sounds as courtship signals as well as during agonistic encounters with other males; however, females did not produce sounds (Phillips and Johnston 2008b). This mixture of sound signaling with visual displays ensures that male Whitetail Shiners attract spawning ready mates. Sound may assist in species recognition or mate selection. Phillips and Johnston (2008b) further examined these acoustic signals in populations from Arkansas and Tennessee; they discovered that different populations shared the “same acoustic repertoire (producing knocks, short knocks, and pulse bursts), significant amounts of geographical variation were found.”  Although the disjunct populations were similar morphologically, the acoustic signals were divergent.  

Threats to populations of Whitetail Shiners are not fully studied; IUCN rates them as a “least concern” species.   However, where they do occur they are easy to observe with a mask and snorkel or capture with a minnow seine.   Just don’t dump these or other minnows into non-local streams!

References

Buckwalter, J.D. 2016. Invasion success and species traits of New River stream fishes. Master’s thesis. Virginia Polytechnic Institute and State University, Blacksburg, Virginia. 94 pp.

Burkhead, N. M., and H. Jelks. 2001. Effects of suspended sediment on the reproductive success of the tricolor shiner, a crevice-spawning minnow. Transactions of the American Fisheries Society 130:959–968.

Easton, R. S., and D. J. Orth. 1994. Fishes of the main channel New River, West Virginia. Virginia Journal of Science 45:265-277.

Jenkins, R.E. and Burkhead, N.M. 1994. Freshwater fishes of Virginia. American Fisheries Society, Bethesda, Maryland. 1079 pp.

Mayden, R.L. 1989. Phylogenetic studies of North American minnows, with emphasis on the genus CYPRINELLA (Teleostei: Cypriniformes). University of Kansas Museum Natural History Miscellaneous Publication 80:1-189.

NatureServe. 2013. Cyprinella galactura. The IUCN Red List of Threatened Species 2013: e.T202079A15364032. http://dx.doi.org/10.2305/IUCN.UK.2013-1.RLTS.T202079A15364032.en. Downloaded on 04 January 2016.

Phillips, C.T., and C.E. Johnston. 2008a.  Sound production and associated behaviors in Cyprinella galactura.  Environmental Biology of Fishes 82:265-275 DOI 10.1007/s10641-007-9279-5

Phillips, C.T., and C.E. Johnston.  2008b. Geographical divergence of acoustic signals in Cyprinella galactura, the whitetail shiner (Cyprinidae).  Animal Behaviour 75:617-626. doi:10.1016/j.anbehav.2007.06.022

Sutherland, A.B. 2007. Effects of increased suspended sediment on the reproductive success of an upland crevice-spawning minnow. Transactions of the American Fisheries Society 136:416-422.  DOI: 10.1577/T06-046.1

Sutherland, A.B., and J.L. Meyer. 2007. Effects of increased suspended sediment on growth rate and gill condition of two southern Appalachian minnows.  Environmental Biology of Fishes 80:389–403 DOI 10.1007/s10641-006-9139-8