'Electric eels have a strategy for inactivating the muscles of difficult, struggling prey that have been grasped but not subdued. In these cases, the eels concentrate the electric field by sandwiching the prey between the two poles of their long electric organ'.*
The remarkable physiology of the electric eel (Electrophorus electricus) made it one of the first model species in science. It was pivotal for understanding animal electricity in the 1700s, was investigated by Humboldt and Faraday in the 1800s, was leveraged to isolate the acetylcholine receptor in the 20th century, and has inspired the design of new power sources and provided insights to electric organ evolution in the 21stcentury. And yet few studies have investigated the electric eel’s behavior.
This review focuses on a series of recently discovered behaviors that evolved alongside the eel’s extreme physiology. Eels use their high-voltage electric discharge to remotely control prey by transcutaneously activating motor neurons. Hunting eels use this behavior in two different ways. When prey have been detected, eels use high-voltage to cause immobility by inducing sustained, involuntary muscle contractions. On the other hand, when prey are hidden, eels often use brief pulses to induce prey twitch, which causes a water movement detected by the eel’s mechanoreceptors. Once grasped in the eel's jaws, difficult prey are often subdued by sandwiching them between the two poles (head and tail) of the eel’s powerful electric organ. The resulting concentration of the high-voltage discharge, delivered at high-rates, causes involuntary fatigue in prey muscles. This novel strategy for inactivating muscles is functionally analogous to poisoning the neuromuscular junction with venom. For self-defense, electric eels leap from the water to directly electrify threats, efficiently activating nociceptors to deter their target. The latter behavior supports a legendary account by Alexander von Humboldt who described a battle between electric eels and horses in 1800. Finally, electric eels use high-voltage not only as a weapon, but also to efficiently track fast-moving prey with active electroreception
*Abstract from Catania K.C. (2019) The Astonishing Behavior of Electric Eels. (2019). Front. Integr. Neurosci. 3:23.
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
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