Aphis nerii, the small cows of the ants

Domain: Eucaryota, Kingdom: Animalia, Subkingdom: Eumetazoa, Phyllum: Artropoda, Subphyllum: Hexapoda, Class: Insecta, Subclass: Pterygota, Order: Hemiptera, Suborder: Sternorrhyncha, Superfamily: Aphidoidea, Family: Aphididae Latreille, 1802. Subfamily: Aphidinae Latreille, 1802, Tribe: Aphidini Latreille, 1802, Subtribe: Aphidina Latreille, 1802, Genre: Aphis Linnaeus, 1758, Species: Aphis nerii Boyer de Fonscolombe, 1841. Such is the complicated international taxonomic classification of this little animal sucking sap, the oleander aphid, a tiny insect chubby soft body and translucent yellow measuring between 1'5 and 2'66 mm. in adulthood.

 Aphis nerii on an immature fruit of oleander, Nerium oleander. (I recommend expanding this and the following pictures to better appreciate the details).

Generally parasitic plants of the Apocynaceae family (Nerium and Vinca) and the discussed family of the Asclepiadaceae (Araujia, Asclepias, Calotropis, Caralluma, Cynanchum, Gomphocarpus, Periploca and Vincetoxicum), which according to recent studies on genetic be actually a subclade within the Apocynaceae. Occasionally plants can also infest families Compositae, Convolvulaceae, Euphorbiaceae and some of Rutaceae of Citrus genus and, as discussed below, is also able to feed on the sap of some exotic plants not Mediterranean of the Cactaceae family.

Video capture of Aphis nerii  aphids viewed under a microscope at 40x magnification.

Aphis nerii in early May on a flowering branch of oleander, Nerium oleander, together with an old waterwheel Guadalquivir River as it passes through the city of Cordoba.

Colony of aphids in mid-September on a oleander of the Majorcan town of Soller.

All of the aphids Aphis nerii Mediterranean region are parthenogenetic viviparous females, ie reproduce asexually by parthenogenesis without the fertilizing males, since there are no examples of this kind male outside Japan. In this Asian country aphids of the first generations of the annual cycle are all parthenogenetic females and no males, just as in the Mediterranean, but in the last generation Japanese autumn all aphids are sexed and winged males and females, so there is a theory that places the origin of this species of aphids in the Japanese archipelago. There also are viviparous females in the first year and oviparous generations in the last generation, just as the winter cold starts. Then the last female of the annual cycle, after being fertilized by a male fly in search of a plant in which to deposit their only big egg sticking a flower or vegetative bud, which will hatch the following spring. After laying eggs all adult aphids, males and females, die struck by the cold.

The Mediterranean aphids, by contrast, are viviparous in all generations. The latest annual cycle autumn females do not lay eggs. To overcome the winter, after going through the four stages and the five nymphal molts its exoskeleton and maturity, just hide and go into hibernation.

Previous aphids of different ages. They are the remnants of cuticle molting, these insects carried five times during their life.

The curious life of the Mediterranean Aphis nerii begins in spring when adult aphids recent previous cycle wake of winter dormancy, after spending the harsh cold months in hibernation under leaves and crevices of the bark of the oleanders. Then the autumn survivors aphids rise to new outbreaks of oleander spring and feed on the juicy and nutritious sap of parasitized plant and a few days, and good fat, they give birth to small female aphids genetically identical to their mother , ie clones with the same genome, which, after passing through four nymphal stages and five changes, reach maturity.

The aphids of second generation, all wingless, ie without wings surround their mother forming a colony and are getting fat and shedding its cuticle as they grow. At maturity, like their mother, they give birth to living daughters parthenogenetically, most wingless and winged a few, depending on the saturation of the colony of aphids. Individuals winged parthenogenetic females and apterous specimens, looking fly without parasitize shoots of the same plant or nearby plants and form new colonies, which, when they reach maximum saturation capacity of individuals, generate a more or lower number of winged females that  leave the colony in search of new territories. So are happening generations of aphids during the warmer months of spring, summer and early fall Mediterranean.

When it starts to cool, about mid autumn, oleander aphids know they can not survive the cold still active or awake and art becomes hibernating. Thus, entering winter dormancy, paralyze their metabolism, sleep and wait. When at last the first rays of spring temperature increase, the body's lymph overwintering aphids warms, their metabolism is reactivated and awaken again to the adventure of a lifetime. Survival of the species depends on the few adult aphids that have survived the long and treacherous Mediterranean winter and the many predators, especially insectivorous birds, who have eagerly sought under the leaves to feed on them.

Detail of previous aphids on the underside of a leaf. Striking preference for the midrib and secondary veins of the leaf, which are juicier feeder vessels to sink its proboscis stylet  and suck the sap of the phloem. Being the parasitized plant juices high in sugar but low in protein aphid is forced to suck more sap that it need to get the essential aminoacids necessary for its metabolism. For evitate the flood its body with many sugars, they eliminate the excess juices by the anus located below the organ called cauda in the back of the abdomen. The fluid excreted is rich in carbohydrates, has a honey-like consistency and therefore called molasses.

 Aphis nerii on an oleander immature fruit in mid-September.

The honeydew excreted through the anus is a delicious treat for many insects, especially ants, which establish an alliance with aphids, a symbiosis, a mutual partnership, in which both insects make a profit. In return for honeydew droplets, the ants protect the aphids from predators, clean their bodies, removed the dry casings of its five sheddings and move the newborn aphids to other no parasitized parts of the plant, ie they act as true shepherds who feed the dairy cows, goats or sheep and move them to new pastures to eat better. This symbiosis between ants and plants is very common in nature and called myrmecophily.

The aphids Aphis nerii can also parasitize other plants, as this cactus called Neobuxbaumia polylopha native to Mexico, cultivated in the magnificent Soller Botanical Garden. The photographs were taken in mid-September.

Flower detail above, it is already past and closed after the previous day be pollinated by wasps and bees, with many aphids sucking the sap.

Same previous aphids from more close.

There is another theory which places the origin of the aphid Aphis nerii in the Mediterranean region, as well as its main host plant, oleander, but the absence of males in the Mediterranean seems to rule out this hypothesis in favor of placing its origin in Japan. Anyway, from the Mediterranean region the aphid has spread slowly hidden under the leaves of the oleander exported as garden plants and currently lives in all regions of the world with a subtropical and temperate similar to warm their home. With no need for any male to breed, just to be "exported" one female one under a leaf to start a new population overseas. Hence, all the copies that have invaded new territories outside the Mediterranean are all viviparous parthenogenetic females of Mediterranean origin. It has not been the same with the subspecies Japanese male and female oviparous in autumn generation, as it has not been found any male Aphis nerii outside Japan.

And now comes a question: should the Mediterranean subspecies of a Japanese female who for many years managed to leave the Japanese archipelago, perhaps in a bonsai as a gift sent by the Emperor of Japan to Emperor of ancient Persia and, finding no male, had to resort to the strategy of parthenogenesis to reproduce asexually even in the autumn generation, filling clonic daughters of the beautiful oleanders Hanging Gardens of Babylon?. Hence reaching the Mediterranean coast could be just a matter of a couple of centuries. This would explain why the same species, in the autumn generation in Japan reproduces sexually with males and females, while in the Mediterranean only parthenogenetic females throughout the annual cycle.

The tender stems of the Asclepiadaceae, as this Vincetoxicum of Menorca pink flowers yet unidentified, are also victims of the parasites of aphids Aphis nerii.

In this picture you can see the actual size of these aphids when compared with the tip of my index finger.

Interestingly the aphids respect the flowers and allow the Vincetoxicum bloom and fruit smoothly.

Some anatomical details of the aphid.

Aphis nerii viewed under a microscope at 40x magnification. Its body is formed by a head with two long antennae, two black eyes in lateral position and a mouth as a proboscis with a stylet in the end specialized to drill plant tissue, a thorax consists of three segments, in each one of which exits at the bottom a pair of articulated legs black color and covered with hairs and on top of the second and third segment there are a pair of wings in  winged individuals, more larger the first pair and finally at its posterior part a bulky abdomen with two siphons black color directed upwardly and an anal plate at the rear end where is located a tubular black organ rearward as a queue, called cauda, with the anal opening just below this caudal organ.

Detail of the body parts of an oleander aphid.

Aphid with a drop of wax coming off one of its two siphons. These waxes are rich in volatiles, especially pheromones that maintain the colony members united and gases repellents to ward off predators.

Aphids Aphis nerii can impair severely parasitized plants, although rarely get killed. They can also be transmitters of viruses between plants through its stylus, the contaminated biting an infected plant and then fly to a healthy plant and spreading the virus. By not parasitize plants producing food, not usually combated with pesticides and is very easy to find their colonies on the oleanders planted in the public and private gardens and on roadsides.

An Asclepiadaceae of beautiful flowers, the Asclepias curassavica, native to tropical America and cultivated worldwide as an ornamental plant, it is also parasitized by aphids Aphys nerii.

 Asclepias curassavica fruits covered with aphids.

Detail of previous aphids.

In natural conditions its colonies are controlled by numerous predators that feed on aphids, such as lady beetles in the family Coccinellidae, some Diptera as the larvae of hoverflies of the Syrphidae  family and some Neuroptera of Chamaemyiidae, Chrysopidae and Hemerobiidae family.

One of the most effective predators of aphids combat oleander is a parasitoid wasp native to South America, the Lysiphlebus testaceipes of the Braconidae family, which was introduced in North America and the Mediterranean as a biological control agent. The female of the species deposit a single egg inserting the ovipositor into the body of an aphid. When the egg hatches the newborn larva of the wasp feeds on the internal organs of the host, which swells and hardens, becomes mummified. Finally, when the body of the aphid has been completely consumed, the larva metamorphoses into a new parasitoid wasp that emerges from the back of the abdomen of the aphid drilling a hole in the exoskeleton of the host.

 

 Two aphids with droplets of volatile waxes in their siphons. On the right are the remains of dry exoskeleton after the shedding.

The aphids Aphis nerii can extract cardiotoxic substances called cardenolides from the Asclepiadaceae who they infest. These substances are bitter and dissolved in molasses secreted by the anus of the aphids. Also focus on the aphid body without it affecting him at all. The bright yellow color associated with the toxin content is an example of aposematism (ability to repel predators through brightly colored (eg, yellow and / or red on black in wasps, frogs and snakes), fearsome thorns, fangs, stings, etc ...). Both the yellow color of its body like waxes excreted through the anus protect them from the depredations of some species of birds and spiders. It has also shown that the cardenolide act as an effective deterrent against predators such as certain neuropters and ladybugs. No information on the effect of these toxins on parasitoids wasps.

                  

PS: I want to thank the invaluable help of Mr. Angel Umarán, naturalist, photographer and expert in aphids. Without his accurate corrections this article had contained unforgivable scientific inaccuracies. Thank you, Angel!

Tetraclinis articulata, a treasure from Murcia, relic of Late Miocene

The Strait of Gibraltar separated it from its African sisters.

The Sabina mora, Araar, Cypress of Cartagena, Sandarac, etc ...with scientific name Tetraclinis articulata, is a small conifer of Cupressaceae family with tall of shrub generally, although in highly concessional conditions can reach 16 meters in height and a trunk thickness of 1.2 meters. It is the only species of the genus Tetraclinis.

 

Tiny newborn Tetraclinis articulata  in September 2005. About 9 years ago a young man from Cartagena visited my garden website and he looked for a picture of this Iberian-african endemism beloved by Murcian  botanists, but found none. Then looked at the list of my garden plants and found that there was no copy of this beautiful conifer. Something angry he wrote me an email offering Tetraclinis articulata seeds of Cartagena, because "I want that you have an endemic plant of Murcia in your garden," he said. A few days later I received an envelope with 4 seeds of Araar.

 Of the 4 seeds that the young man sent me (that if one day read this article I want to know that is dedicated in gratitude for their generous gesture) three seedlings germinated in March, of which only one survived. Now with over 7 years of age has become a tree of more than three meters high, which is growing fast and seems very comfortable rooted in the rocky, chalky soil of Mallorca.

The botanist who gave the name knew summarize in two female words the essence of its anatomy. The Latin name of the genus Tetraclinis comes from the union of two Greek words, κλινα and τετρά, meaning four beds, for the four scales concave form of the strobilus off and remember the old couches (triclinium) of Romans. (From κλινη, κλινης = bed comes some actual words of our language, as recline, incline, decline, clinic, clinometer, triclinium, etc. ..). The species name, articulata, refers to the peculiar arrangement of the twigs loose like pieces joined or articulated at their ends. 

"Articulated" twigs of Araar tree.

The current distribution of Araar in the southeast of the Iberian Peninsula (Cartagena Mountains in the province of Murcia), in North Africa (Morocco, Algeria, Tunisia and Melilla) and small places on the island of Malta and the island of Cyprus speaks clearly of its Miocene origin. A curious fact was discovered in 1997 a group of 24 centenarians Tetraclinis articulata in the Doñana National Park, specifically in the Coto del Rey in Hinojos (Huelva), some up to 16 meters in height and a trunk circumference of 2 ' 62 meters, much larger than those of Cartagena. Given its age, its size and the absence of signs of having been planted by man, it follows that they are natural, a vestige of what were great forests of Tetraclinis before intense deforestation at the hands of man.  Tetraclinis articulata in Doñana.

 Cypress of Cartagena 7 months old in March 2006. It shows very well how it are changing the leaves as it grows. The former, who wear the stem, are long pointed needles as any conifer. In each new sprouting are becoming shorter to insignificance in their adult phase, as seen in the photo twigs articulated above. The tree performs photosynthesis directly on green twigs. These two phases in the foliation, with juvenile foliage and adult foliage, are typical in conifers of the Cupressaceae family: Juniperus, Cupressus, Thuia, Chamaecyparis, Platycladus ...

The Mediterranean Sea, a direct descendant of primitive Tethys Sea, almost completely dried about seven million years ago during the Messinian great salinity crisis of Late Miocene which took about a million years, during which the sea water is evaporated and salts were deposited on dry sand, desert valleys becoming lifeless what had once been a rich seabed. The cause of desertification was a sudden climate change that much the Earth cooled and made fresh water to accumulate as ice on Antarctica, covering it with a thick layer of water ice several kilometers thick, which caused a decrease significant rains across the globe and of course also in the Mediterranean and a decrease in sea level of over 100 meters.

 

Same Araar at 4 years old in November 2009.

To coincide with the global cooling there was a sudden movement of the African tectonic plate, which, in its continuous ascent northward from which separated the great southern continent Gondwana, collided violently with the European tectonic plate and as a result of this collision is raised the seabed, forming the Betic-Rif Massif which closed the communication between the Atlantic Ocean and the Mediterranean Sea. The reduced rainfall and cessation water ingress to the Mediterranean ocean engulfed in a gradual drying process by simple evaporation and in a few millennia became a very salty sand desert with some caustic lakes in the lower parts.  Toward these lakes came flocks of pink flamingos from Africa and Asia to feed on small halophilic invertebrates and algae living in its  brackish waters.

Approximate boundaries Betic-Rif Massif during the late Miocene in full Messinian salinity crisis with very salty lakes occupying the lower parts of the seabed of the Mediterranean Basin. The brackish lake size depended on the scant rainfall, reaching to dry completely for several millennia. In the mountaintops rains were more generous than in the deep valleys whose sandy soil was covered by a thick layer of salt.

During this million years what had been mountains became islands and coasts of Europe and Africa came together in a continuum without water than separated. It was then that many plants and animals European, African and Macaronesian could expand their populations and occupy all that vast region. Cypress Cartagena, our Tetraclinis articulata, from its native Africa colonized the mountains of Betic-Rif Massif, settling in warmer mountain slopes facing south.

 Current distribution of known indigenous populations of Tetraclinis articulata. In southeastern Spanish small feral populations exist outside Murcia, especially in Malaga and Alicante, which are products of ancient repopulation.

At the end of the Messinian period about 6 million years the Earth suffered a new climate change with global warming that increased rainfall across the planet, melting much of the Antarctic ice and rising water level of the oceans in more 60 meters. At the same time there was a new tectonic movement and European and African tectonic plates separated and Betic-Rif Massif split in two forming a deep groove, the Strait of Gibraltar, which again allowed the entry of oceanic water into the Mediterranean, forming an impressive waterfall drop of several kilometers and a flow of millions of tons of water per second, which quickly filled the Mediterranean in just about 1000 years.

Same Araar tree of 7 years old  in September 2012 with a height of over three meters. Its affection for the sunlight makes grow it inclined toward the midday sun.

What during the Messinian period had been some mountains surrounded by a brackish desert became current Mediterranean islands, isolated again by seawater. The plants and animals that lived in them were isolated from other populations of the same species, as happened to the conifer Tetraclinis articulata, surviving to the present day as relics of those turbulent prehistoric times.

Tetraclinis articulata male strobili in November. This tree is monoecious with separate male and female flowers on the same plant.

Tetraclinis articulata female flowers on the same copy before.

Detail of a female flower of Tetraclinis articulata.

Combined photography with male and female flowers.

Fruits of Tetraclinis articulata about to mature in August.

Details of previous fruits.

Mature fruits in mid-September. The four scales of the strobilus are opened to release the winged seeds.

Fruits of Tetraclinis articulata with flakes shaped as roman kneelers.

Tiny seeds of Araar tree shaped as winged samara, flying like small helicopters windblown to colonize new territory away from his mother.

The Sabina mora is much appreciated in gardening, though still a rarity in private gardens. May be reproduced by grafting on Thuia and Cupressus. It is grown successfully in all the Spanish Mediterranean botanical gardens. In Murcia have made numerous reforestation to increase its range. It is the national tree of Malta which is called Sandarac gum tree in English and gharghar in Maltese. Its Araar name comes from the Arabic and so is commonly called in North Africa.

Genetic studies have been made of the copies from Murcia and results were compared with the genome of the North African, Maltese and Cypriots trees. Surprisingly no significant differences were found. It follows that the cupressaceae Tetraclinis articulata presents a great homogeneity and genetic stability, despite their different populations carry six long separated million years.