In his book "The voyage of the Beagle", Charles Darwin set out the framework of a theory for the formation of lagoon-islands, atolls, and reefs. It started with a coral reef formation around an extinct volcanic island, growing from a fringing reef to a barrier reef to an atoll, as the island and ocean floor subsided. Since Darwin's discovery, many have wondered how rich and diverse ecosystems teeming with fishes like coral reefs could grow in the marine equivalent of a desert. Some even called it the ‘Darwins paradox’. But is it really a paradox? Evolution basically describes how complex and rich forms of life developed from very elementary organisms and mechanisms. And even an empty ocean may not be the barren desert some take it to be.
The basic mechanism of coral growth is the symbiosis between the coral polyps and symbiotic algae called zooxanthella stocked in the tentacle of the coral polyps. The algae provide the carbon necessary to build up the skeleton of the coral. The coral polyps also extract nutrients like nitrogen and plankton from the seawater to provide the algae carbon dioxide and phosphates. Some marine biologists believe that the phytoplankton may be the primary source of the development of coral ecosystems. The enhancement in phytoplankton near an island-reef ecosystem is also called the Island Mass effect (IME, see insert).
This paradoxical enhancement in phytoplankton near an island-reef ecosystem was discovered about 60 years ago by Doti and Ogury, and recently confirmed by Jamison Gove. He and his team showed that IME is an important feature among a majority of coral reef ecosystems surveyed, creating near-island ‘hotspots’ of phytoplankton biomass throughout the upper water column. The team supervised by Jamison found phytoplankton coral island hotspots surrounded by barren oceans landscapes were nearly everywhere the team looked. Apparently, corals have an astonishing capacity for storing scarce nutrients for their survival. They pick up phytoplankton from the surrounding currents or rising from deeper colder layers around the island to feed the algae that that provide nutrients for the growth of corals using photosynthesis.
A recent study by Simon Brandl published in Science suggests that the ocean’s smallest vertebrates, called cryptobenthic reef fishes, promote internal reef-fish biomass production through exceptional larval supply from the pelagic environment. In addition to the phytoplankton, these tiny fishes and larvae form an important nutrient for larger fishes such as smaller coral fishes and even pelagic predators of the coral reef. So they could also provide (indirectly) the energy and fuel for species on the reef higher in the food chain. Finally, sponges and their excrements also seem essential for the energy cycle, providing ‘manure’ for the coral reefs as well as food for smaller species like crabs, worms, and snails.
Like other top ocean predators, the sea otters presence helps to maintain a diverse community of animals and plants in the kelp forests. Otters eat sea urchins and other grazing animals such as crabs and abalones keeping them from devouring the kelp. Once hunted to extinction for the fur trade, the southern thick-haired sea otter (Enhydra litris nereis) has had a slow road to recovery under more than a century of legal protections. Last year it even reached a number of almost 3200 species. The sea otter profited from the sea urchin boom along the Californian coast, but now shows a jump in mortality that curtails their expansion. The reason is bites from great whites, who are also growing in number due to their pinniped food source expanding. Instead of preying on the otters (they don’t have the blubber of other sea mammals) sharks are taking investigative bites, some of which cause severe injuries causing death
A sea otter research program is carried out in Monterey Bay Sea Aquarium led by Michelle Staedler using data loggers to track their goings, and rescuing abandoned otters. Because of the increased risk of shark bites, researchers as Kerstin Wasson and Ron Eby are now exploring new shark-free habitats for the otters. One such area is Elkhorn Slough, a major estuary system in Moss Landing that feeds into Monterey Bay. Although the swampy slough is not really a coastal area, the otters so far seem to enjoy their new habitat where they also have more opportunities to stay on land. Captured abandoned sea otters from the Monterey coast are also released in Elkhorn Slough by Michelle Staedler and her team.
Eelgrass beds in the Slough were being smothered by algae that grew unchecked on the leaves, absorbing the sunlight eelgrass needed for photosynthesis. Snails, slugs and other invertebrates would eat the film of algae, cleaning the grass and allowing it to get the sunlight it needs. The snails and slugs, however, tend to be devoured by the increasing number of crabs in the estuary, which have few natural predators. Since the sea otter turned up (now counting around 150 individuals) and began feeding on the crabs (see insert) the balance is now improving. The bay of the San Francisco is another area that Wasson and Eby are exploring as a future shark free habitat of the otters, a place where many sea otters lived in the past until they were killed by fur hunters.
The cuttlefish (Sepia) belongs to the family of Sepiida, that in turn are part of the Cephalopoda which also include squids octopuses and nautiluses. Cuttlefish (see also my earlier Blog) form an enormous variety of species of which some, like Sepia officinalis and Sepia elegans, have -sadly enough- gained great popularity as appetizers and tasty entries on dinner tables. Sepia has a cuttlebone used for buoyancy control. They feed themselves by extending two hidden feeding tentacles, which snag prey and pull it back to its strong beak. When Sepia mates the male grabs the female by the face and inserts a specialized tentacle into an opening near the females’ mouth and then inserts sperm sacks. The male then guards the female until the eggs are laid a few hours later.
Giant Cuttlefish (picture taken by Dave Abbott)
The reputation of Sepia as ‘ chameleon of the sea’ is based on their unique capacity to rapidly change color by controlling pigment cells in their skin. Their skin functions like an extended brain, a bit like the eight arms of the Octopus, with two-thirds of its nerve cells located in the nerve cords of its arms (see my earlier Blog on Octopus). But in Sepia, the brain is reflected in its pigment carrying cells in the skin. These chromatophores produce colors varying between orange, red, yellow, brown or black. They are like color pixels on a computer screen, but instead of a computer program their skin cells are controlled by motor neurons in the brain, that in turn activate muscles around the chromatophores. The muscles constantly expand and contract in a complex choreography in direct response to the activity of motor neurons, which is displayed in rapid changes in the color of the chromatophores.
The color changes reflect the inner state of the cuttlefish. They may mirror certain ‘emotions’ like fear (for predators), sexual attraction (spotting a potential partner), anger (spotting a rival) or when using camouflage by mimicking the color seagrass of coral. The mating ritual of the Australian giant cuttlefish is particularly impressive with respect to color changes.
Groups of cuttlefish use complex codes, changing rapidly in often synchronous patterns of pigment changes reflecting processes of social communication, of which the meaning still remains a mystery for biological science.
Sam Reiter and his team from The Max-Planck Institute for Brain research, recently published an article in the journal Nature, describing in more detail the properties of cells in the cuttlefish skin, and neurons extending from the brain that control color changes. The team monitored changes in the state of the color-changing cells in living cuttlefish with high-resolution cameras, which allowed them to track the activity of tens of thousands of neurons simultaneously, for the first time. They also used electrical stimulation of muscles of the mantle of a small number of cuttlefish to produce artificial color changes and track motor units (nerve cells that make a muscle contract). Analysis of the pattern dynamics and rules that govern the development of skin pattern, showed that new pixels of the chromatophores (that changed recently) were mostly yellow and more mature pixels black.
Green sea turtles (Chelonia mydas) migrate long distances between feeding and nesting sites; and some swim more than 2,600 kilometers to reach their spawning grounds. Female turtles can store sperm from a single mating for the entire nesting season and males visit the breeding areas every year, attempting to mate. The eggs are round and white, and about 4-5 cm in diameter and hatch in the sand. The hatchlings remain buried until they all emerge together at night after around two months.Then they rush instinctively over the beach to the waterline. Nests may contain up to 200 eggs. But only few turtles reach adulthood in the oceans where they are a favorite prey for various predators. The highest rate of predation occurs in the water within the first 30–60 min of swimming as they pass through the cordon of predators found in the shallow water surrounding natal beaches
Left: Top: two separate nesting sites of green sea turtles along the Great Barrier Reef. ( adapted from **).
Along the east coast of Australia female and male green turtles mate in the vicinity of their nesting beach. The Northern Great Barrier Reef (GBR) is home to one of the largest green turtle populations in the world, with an estimated female population size of around 200,000 nesting females. Furthermore, two genetically distinct breeding populations of green turtles are found at the opposite ends of the Great Barrier Reef: the southern Great Barrier Reef (sGBR) stock and the northern Great Barrier Reef (nGBR) stock, with virtually no nesting occurring along the middle part of the GBR (see picture left). On the average 80% of the turtles at the GBR are female and 20% male.
Sex determination in turtles Reptiles are related to birds and have roamed the earth for more than 300 million years. Most reptiles including sea turtles do not have sex chromosomes. Instead, sex of newborns depends on temperature-dependent sex determination (TSD). TSD relates to temperatures experienced during the middle third of embryonic development. It was already known to hold for the green as well as the painted turtle (Chrysemys pica) populations in areas where cooler summers always produced mostly male, and warmer summers mostly female turtle offspring (see Janzen *). Janzen also found that nests of the common snapping turtle (Chelydra serpentina) incubated at 26°C produced 100% males, at 30°C produced 100% females, and at 28°C produced equal numbers of females and males.
How does TSD work? Pivotal temperatures are species-specific temperature ranges in which males and females are produced in equal number. The pivotal temperature is heritable but only a few degrees Celsius are needed to drastically alter this ratio to produce 100% males or 100% females spans. It still remains unclear how the developing embryo detects a thermal stimulus that apparently directs its sexual fate. Microscopic studies of the embryo gonads have established that steroid hormones could start the process once the temperature change is detected. In some turtles the critical temperature-dependent component appears to be synthesis of the enzyme aromatase, which converts androgens, such as testosterone, into estrogens. At higher temperatures, increased aromatase activity produces more estrogens, which biases the sex ratio toward more females.
TSD and fitness A common pattern of TSD in turtles is that warmer temperatures favor development of female and colder temperatures development of male hatchlings. This pattern would make sense from the point of view of natural selection if females gain more in lifetime fitness by developing in higher water temperatures compared to male turtles. Which would create a stronger tendency of females than males to avoid cooler beaches. For example, warmer temperatures may lead to a stronger greater adult body size, which has a greater effect on female fecundity than on male fertility. In line with this theory Janzen reported that hatchlings from the all-male and all-female producing temperatures had significantly higher first-year survivorship than did consexuals from the incubation temperature that produced both sexes from the incubation temperature that produced both sexes.
Climate warming and GBR nesting Species with TSD have existed for millions of years and coped with the selective pressures of a changing environment through adaptive changes of heritable traits. However, it is unlikely that these traits would evolve rapidly enough to keep pace with the current rate of climatic warming. A recent Australian/American study carried out on 441 green turtles of the GBR (**) has shed more light on the possible impact of climate change on changing sex ratio’s of the green turtles colonies of the GBR. Blood and tissue samples were collected from the turtles to determine sex, steroid hormones and DNA. The study found a strong sex bias depending on the location of the GBR where eggs hatched. In the cooler southern GBR nesting beaches there was a moderate female sex bias (65%–69% female) in turtles, but turtles that originated from northern GBR nesting beaches were extremely female-biased (99.1% of juvenile, 99.8% of sub-adults, and 86.8% of adult-sized turtles; see also figure above, lower panel). The study further indicated that northern GBR green turtle locations have been producing primarily females for more than two decades and that the proportion of females has increased in recent decades.
Conclusion With average global temperature predicted to increase 2.6C by 2100, many sea turtle populations are in danger of high egg mortality and female-only off-springs. A high female bias as such might not create a problem, since only few males are needed to fertilize an entire colony of females. But an extreme female bias would create a problem in finding a male at all, and/or lead to genetic impoverishment due to lack of genetic variation in a relatively small group of males. Visits of breeding males from other populations might mitigate extreme feminization, but this would be less likely to occur at the northern GBR, where visits of male turtles from the south are less likely to occur.
Extreme incubation temperatures not only produce female-only hatchlings but also cause high mortality of developing clutches. A some beaches in Florida the strain of surviving at elevated temperatures and resulting heat stress seems to weaken the hatchlings and slow down their run to reach the shoreline in time. Researchers are now exploring plans to cool the nests, like using shade cloth or putting water on top of them.
*Janzen, F.J. (1994). Climate change and temperature-dependent sex determination in reptiles. Proc. Natl. Acad. Sci. USA 91, 7487–7490.
Janzen,F.J. (1995) Experimental evidence for the evolutionary significance of temperature-dependent sex determination, Evolution 49 864 – 873.
**Jensen, M.P. et al. (2018), Environmental Warming and Feminization of One of the Largest Sea Turtle Populations in the World. Current Biology 28, 154–159
***Spencer, R. J.; Janzen, F. J. (2014). "A novel hypothesis for the adaptive maintenance of environmental sex determination in a turtle". Proceedings of the Royal Society B. 281
Hake, L. & O'Connor, C. (2008) Genetic mechanisms of sex determination. Nature Education 1(1):25
Warner DA, Shine R (2008). "The adaptive significance of temperature-dependent sex determination in a reptile". Nature. 451(7178): 566–568. .
Pen, Ido, et al. (2010). "Climate-driven population divergence in sex-determining systems". Nature. 468: 436–439.
Valenzuela, Nicole; Fredric J. Janzen (2001). "Nest-site philopatry and the evolution of temperature-dependent sex determination" (PDF). Evolutionary Ecology Research. 3: 779–794. Retrieved 7 December 2011
Mrosovsky, N., and Yntema, C.L. (1980). Temperature dependence of sexual differentiation in sea turtles: implications for conservation practices. Biol
Luckily our world is still full of birds and insects that produce a variety of sounds. Even the sounds of some insects are pleasant to listen to. Like the songs of crickets and the Cicadas or Cigales of the Provence in France. The male cicadas can produce exceptionally loud sounds by using two small membranes under each wing that vibrate rapidly when pulled by tiny muscles. The male abdomen is largely hollow, and acts as a sound box, similar to a cello instrument. On hot summer days whole groups of males congregate in the plane- or pine trees and synchronize their sound to establish chorusing centers that fill entire streets or market squares. The reason why is to attract the females. And perhaps also to entertain the summerguests having lunch under the pine trees with a glas of cold vin rosee within reach.
..Oops, almost forgot that this is about fishes not cicadas! In contrast with birds and insects the reputation of fishes is not mainly based on the sounds that they make. Nevertheless, many fishes in the Atlantic or tropical oceans create different types of sounds using different mechanisms and for different reasons. Research of sound production in fish is still in its infancy. But scientists using recorded fish vocalizations with underwater microphones have identified many fish species that make amazing sounds, either as individuals or in groups. Based on this evidence, it now seems that hundreds of species of marine (and probably also freshwater) fishes are capable of generating acoustic signals
Left: Upper figure: the sound producing mechanism of the catfish in the base of its left pectoral fin (source **). Lower figure: swimbladder (SB), sonic muscle (SM) and sonic nerve (SN) in the northern searobin (adapted from ***)
Active sound production in fish often depends on time and space. Many fishes become ‘talkative’ in the breeding season, following a seasonal and/or diurnal cycle. In contrast with the sophisticated sonar sounds of marine mammals like whales and dolphins, the vocabulary of fish species is limited, and meant to communicate gross information. It could signal danger, distress, competition or attracting a female. Fish vocalizations can take a wide variety of forms, including clicks, purrs, grunts, groans, growls or barks. They may be intentionally produced as signals to predators or competitors, to attract mates or as territorial display.
There are globally two ways in which fishes make sounds. One is stridulation: striking or rubbing together skeletal components. Crickets use stridulation, as well as marine catfish and seahorses. For example seahorse species make clicking and/or snapping sounds by rubbing together bony edges of the skull and the coronet, a crown-shaped plate on the its head. These sounds are possibly amplified by the swim bladder. Some marine catfishes (Arius felis and Bagre marinus) have specialized pectoral fin spines that make a stridulatory squeaking sound. They do so by rubbing the base of the pectoral fin spine against the pectoral girdle (see picture above). The sound can even be heard at the surface by anglers. Trigger fishes can produce drumroll sounds that result from alternate sweeping movements of the right and left pectoral fins, which push a system of three scutes (bony scales) that are forced against the swimbladder wall. Other fishes use their swim bladder to produce sounds. A muscle attached to the swim bladder called the sonic muscle contracts and relaxes in a rapid sequence (see picture above). This action causes the swim bladder to vibrate and produce a low-pitched drumming sound. Examples are the goliath grouper, black drum, toad fish and silver peak. Not to forget the oyster toadfish, that is able to contract its muscle at a rate of 200 times a second. The swim bladder can either function as the actual sound generator itself, or as an amplifier for sounds generated by other body parts including e.g. the pectoral girdle, fin rays, various other bones or tooth in front of the mouth.
Along coral reefs of the Red Sea clownfish, triggerfish, damselfish and angelfish often make loud clicks, drum rolls, or ‘pangs’ during agonistic interactions, in distress and or when divers get too close to their territory (see audio gallery). Other male fishes, mostly found in the greater oceans or their coastlines are known to create very strange and often very loud sounds. The sounds mostly serve to attract females in the mating or spawning seasons. Here follow examples of some notorious sound producing species.
Catfish Catfish can become very large and are found in the sea, coastal water and rivers. The squeeker catfish (Synodontis eupterus) make a croaking sound by rubbing the spines located in their pectoral fins into grooves on their shoulders as shown in the picture above. Talking catfish (Platydoras armatulus) can produce sound in two ways—by vibrating their swim bladder or by vibrating their pectoral fin spines in their sockets.
Oyster toadfish (Opsanus tau) is a froglike fish from the family of Batrachoididae. The fish has a distinctive "foghorn" sound used by males to attract females in the mating season (audio gallery and toadfish song). Males make nests, and then attract females by "singing", that is, by releasing air by contracting muscles on their swim bladders. Attracted by the foghorn sound, the female comes into the nest, lays eggs, and then leaves.The sound can be loud enough to be clearly audible from the surface.
Plainfin midshipman (Porichthys notatus) is bioluminescent. The plainfin midshipman is another type of toadfish, found off the west coast of North America from Alaska to Baja California. During the mating season the male midshipman hums—sometimes for long periods—by hitting his swim bladder with his sonic muscle. His humming serves to attract a female. Once she deposits her eggs, the midshipman resumes humming to attract another female to his nest. The male guards the eggs until they hatch. Typically these fishes are nocturnal and bury themselves in sand or mud in the intertidal zone during the day.
The black drum (Pogonias cromis) is a black or greyish fish that lives in the brackish water found in areas such as estuaries. The young fish have black stripes that fade as the fish matures. Black drums are mainly bottom feeders. Adults can become very big and may weigh over a hundred pounds. Black drums become very noisy during the mating season (audio gallery). The low pitched sounds that they produce travel long distances. Again, males produce the sounds to attract females. The fish use their swim bladder and sonic muscle to create the vocalizations. Sometimes black drum mating calls are conducted by the ground and the seawalls and then enter nearby houses on the shore.
Herring communicate with each other by expelling gas from the anal area, producing bubbles and a high-pitched sound. Inventive researchers have called this sound production a FRT (Fast Repetitive Tick). Both the Atlantic herring (Clupea harengus) and the Pacific herring (Clupea pallasii) produce FRTs. The fish swallow air from the water surface and then store it in the swim bladder, so the air is not the result of digesting food. During the night, in darkness and when surrounded by other herring, air is released through the anal duct. The purpose of the collective FRT sounds may be to ensure that the fish stay close together.
Corvina The physical act of reproduction can be a noisy affair for many fishes, but beats all records for the Gulf Corvina (Cynoscion othonopterus). Every spring, millions of these large gray fish migrate to the Colorado River delta and sync their spawning to the tides and the phases of the moon. The magnitude of their sounds (produced by rapidly beating their swim bladders with the sonic muscles) can become even deafening during simultaneous chorusing of males within the larger spawning aggregation. These sounds can even extend up to 27 km distance along the main channel of the Delta and include 1.5 million individuals during a single spawning period. At the loudest the sound level of the chorusing fishes was more than 150 decibels (see corvina). The corvina is endemic to the Northern Gulf of California and faces imminent risk of species extinction due to overfishing of its spawning aggregation, and regulations that allow overfishing to persist*. In the spawning season local fisherman find it easy to locate the fishes by their sounds even from their small boats. With one net they often catch hundreds of corvina’s in a few minutes.
Sources and links
*Erisman BE, Rowell TJ. 2017 A sound worth saving: acoustic characteristics of a massive fish spawning aggregation. Biol. Lett. 13: 20170656
Popper AN, Fay RR, Platt C, Sand O. 2003 Sound detection mechanisms and capabilities of teleostfishes. In Sensory processing in aquatic environments(eds SP Collin, NJ Marshall), pp. 3–28. New York,NY: Berlin, Germany: Springer-Verlag.
Ben Wilson, Robert S. Batty and Lawrence M. Dill 2003. Pacific and Atlantic herring produce burst pulse sounds. Proc. R. Soc. Lond. B (Suppl.) 2003
Discovery of Sound in the Sea. University of Rhode Island and Inner Space Center. http://dosits.org/galleries/audio-gallery/fishes/
http://www.sfu.ca/biology/faculty/dill/publications/,FRTing_herring_Wilson_et_al.pdf (accessed August 26, 2017).