ABSTRACT
This article proposes that loss of phosphorus in Cretaceous soils was the circumstance that caused the vertebrate fauna to decrease in size, bony structure, and teeth on the savannas especially. The loss is proposed to have been caused by addition of phosphorus to erosion susceptible termite runways, especially those of the Amitermitinae (now merged with Termitinae) subfamily. Incomplete evolution of pack hunting by ants, which are the most effective predators of termites today, is proposed as the reason for the overwhelming success of the termites. Phosphorus continues to be a considerable limiting factor in tropical soils in the present world, especially in areas where termites are not kept in check very well by ants, notably Australia.
LINKS
For a discussion of a possible evolution of prototermites in the Triassic from their probable Permian wood roach ancestors, see Permian soil organic content. For a discussion of a proposal that amphibian predators transported phosphorus to Permian oceans see marine phosphorus during the Permian . For a discussion of evolution of termites and ants see termites in the Jurassic and Cretaceous . There is a discussion of the affect of termites on modern ecology and references for this page in the Paleocene and the present.
See this article for speculation as to what causes silica loss as by alkaline guts of termites
INTRODUCTION
When the Cretaceous period began, it was populated by large, well boned, and well armored with bone, terrestrial vertebrates. As the period progressed, there appeared to be a steady decline in size, bony structure, and armor especially outside of South America, and many genera even lost teeth, especially on the savannas. For surface creatures not much constrained by weight, and even those such as birds which are, to lose anything so valuable as bones and teeth is an indication of considerable evolutionary pressure. Teeth are a special liability in phosphorus deficiency because they grow at the same rate [Hawk, 1949] regardless of the phosphorus intake. Not only does this place a strain on the animal, but also they can become subject, as a result, to crowding in the jaw. In addition, teeth don't furnish phosphorus very readily or at all when the body needs to draw on reserves. Perhaps most important of all is that their exposed position makes poorly formed teeth susceptible to infection. A diet which would cause decay in young animals would not harm older animals [Constant, 1954]. A diet deficient only in phosphorus causes rickets [Zucker] [Massry]. In addition it will cause confusion, convulsion and coma in the central nervous system, a decline in red blood cells, leucocytes, bacteriacidal activity, glomerular filtration rate, proximal sodium resorption, several enzymes, and a rise in cell fluid alkalinity [Massry].
I suspect that these bone declines were due to a pervasive phosphorous infertility. I further suspect that this infertility was due to the nature of the erosion as influenced by the rise of the termites (Isoptera) especially the Amitermitinae (now Termitinae) subfamily in monsoon and desert regions. Even at present, termites are the dominant organism in tropical soils, although usually not Amitermitinae outside of Australia.
There are few termite species having less than 1000 individuals per reproductive pair, and most species have well over 10,000 in their colonies. So from this factor alone, their evolution should proceed roughly 10,000 times slower than an equal number of comparable size nonsocial insects since large populations of reproductive units incorporate dominant genes faster than small populations [Wright p139, 142] and large populations would have a greater chance of producing mutations and thus increase variability [Simpson, p119] by cosmic ray bombardment, etc. and a greater chance of being divided into cul de sacs, which last would speed up evolution considerably [Simpson, p123], especially since an individual insect would have a much better chance of being isolated than a cumbersome termite colony. This last would be the case even for flying reproductives to a considerable extent since they do not mate before starting their flight. Furthermore, the reproductives live a decade or more [Keller & Genoud][Wood & Sands p248] some as long as over 65 years [Weesner 1970 p442] and long lived organisms evolve slower than short lived organisms [Smith]. This is substantially more than the year or two that most insects live. It can not possibly be an exaggeration to say that they must be evolving around 10’000 to 100,000 times slower than most other insects when combining these two concepts. Nevertheless, there are over 2700 species of termites. Thus there are somewhere between 27,000,000 and 270,000,000 weighted species of termite vs. 1,000,000 or so unweighted species of all others combined (although ants should be weighted also, of course). This gives some perspective of their importance in the past, and is especially remarkable in view of the small number of saprophagous (eat detritus) insect species. Termites are certainly extremely numerous in the present tropics, said to have as many as 15,000 termites per square meter [Wood 1978] in some places. Furthermore, this analysis ignores the fact that advanced termite species develop secondary reproductives from nymphs if the original queen dies. These reproductives are highly inbred, and this possibly may cut the evolutionary rate in half again for those species. Furthermore, since the queens are replaced by parthenogenesis [Matsuura], her genes are potentially immortal.
Insects associated with termites are also indicative of past success. In spite of the secretive existence of termites and difficulty of living with termites, 700 arthropod species live with them. Most of these are specific for Macrotermitinae fungus growers and Nasutitermitinae that emerge from their underground tunnels. Some succeed by secreting the same odor chemicals that termites secrete, which implies a long coevolution [Howard]. This compares with 2000 coexisting with ants, which latter have a wider range and almost all a more open life. [Roeder, 1953]. Therefore termites must have been very widespread and even more numerous in the past. The fundamentally different designs of the digestive tracts of the several families [Bignell] and the very large number of protective poisons with a completely different chemical configuration [Prestwick 1983, two references for this year] would give further support to this concept.
A type of termite exists in the present world which attains its food by building runways over plants, smothering them, and then eating the dead, decaying material and funguses [Walker 1949] relatively safe from predation. These termites are primarily in the Amitermitinae subfamily (now merged with the Termitinae subfamily) of the Termitidae family. This is the most highly evolved family. It is sufficiently successful in gaining its food this way that it has lost most of its cellulose-digesting protozoa. You may see a picture of twigs encapsulated by them in Wikipedia, It is capable of forming supplementary reproductives, so that it can form extremely large colonies. It may be able to make use of nitrogen recycling funguses [Leach 1940]. If so, this would make possible rapid growth of colonies. Some measure of its success is that there are almost 600 species of Amitermitinae and Termitinae termites.
Its runways are very vulnerable to destruction by rain (Nutting, et al. 1985), so that this strategy would probably be most useful to the termites in monsoon areas and deserts. At least one Amitermitinae that lives in the rain forest makes its nest of wooden material that is resistant to erosion [Malaka 1977]. The present day distribution of termites makes it reasonably likely that this subfamily existed before the close of the Cretaceous since those termites which make their nests in the soil (as opposed to logs or trees) find it almost impossible to cross an ocean barrier much more than 4 or 5 kilometers perhaps because of an instinct to head for the ground after a short time. As already mentioned, their evolution is so slow and their neural patterns and chemistry so extremely complicated that it is virtually impossible that any termite which existed in early Tertiary was not on its way well before the close of the Cretaceous. The Amitermitinae probably arose in the southeast Asian region based on the number of primitive members of the subfamily there [Emerson 1952], most probably Australia. They are the most numerous of the insects in Northern Australia. Other members of the Termitidae arose elsewhere, the Nasutitermitidae, for instance, almost certainly arose in South America [Mayr 1952, p217-225] and the Termitinae relatives of Amitermitinae (Amitermitinae have been now merged into Termitinae) probably in Africa along with more distant cousins, the Macrotermitinae. The Termitidae were thought to be descended from Rhinotermitidae [Weesner] and were almost certainly present in the Cretaceous, therefore. Termitidae prototypes must go back to the Jurassic at least.
If these insects existed in the Cretaceous they must have been extremely successful. Diseases other than funguses are not an important factor, because the colonies seldom intercommunicate but are usually very antagonistic to each other [Kofoid 1934, p23]. For the same reason parasites should be of limited concern to them.
As for predation, their secretive life alone would be sufficient to make them somewhat immune to vertebrate and above ground insectivores. There were no specialized "anteaters" then. Lizards and snakes existed then and eat termites in the present world. However these animals could not have put important pressure on termites in any case since they also eat the termite's chief enemy, the ant, and can not bore into the nest effectively.
The chief enemies of the termite today are the Ponerinae, the Dorylinae, and the Myrmicinae ants [Lee et al 1971]. The blind, subterranean Dorylinae, or army ants, with no flying reproductive queens, can be ruled out on Cretaceous savannas because cosmopolitan members are creatures of the rain forest even today. Furthermore, their distribution makes it unlikely that they existed more than locally in the Cretaceous, probably in South America. I have no data on hand for the Myrmicinae, but it is my perception that they are a modern family. The Ponerine ants are entirely carnivorous and are the most primitive. They are thought to have been derived from the parasitoid wasps in the Triassic or Jurassic [Malyshev 1966 p198-228], most likely the Jurassic. The early Ponerines were supposed to have hunted singly. Those that lived in a colony excavated separate chambers [Haskins 1939]. Some species that hunt in packs extend out onto the savannas in the present Eurasion world, but their distribution makes it clear that it is unlikely that they had these attributes in the Cretaceous.
If the type of ants which do not hunt in packs were the types of ants that coexisted with the Cretaceous Amitermitinae, those termites had a virtually free hand. A single ant could have attacked the termites while in the process of extending their runways and attempt to carry off a helpless worker. However, there were always soldiers presenting their hard, chitinized heads at the opening and when they grabbed they never let go. Against their massed numbers and death grip the ant's superior speed, perception, armor, and poisonous sting were useless. Suicide battalions of termites will fight on to the death even while the breach is being sealed up behind them. A predator, which does not prevail most of the time, can not exploit such a dangerous game routinely.
The desert and monsoon savannas probably came to be subject to severe sheet erosion as a result of the runways of Amitermitinae. Even today in Australia it is estimated that 60 cm of fines were brought up from stones 45 cm of which had eroded [Lee & Wood]. Exposure of topsoil by removal of trees and litter by other termite families along with much less drainage [Spears] because of the decrease in open burrows of other soil creatures toward the close of the Cretaceous probably caused increased runoff from savanna and desert regions compared to the early Jurassic. In addition savanna areas had probably been much extended by the effect of Neotermes on trees. This termite is the only savanna termite that can eat live wood and can reach new sources by boring through the soil. Sometimes it girdles the taproot first, perhaps to avoid drowning in sap or to inhibit production of poisons. Present day distribution of Neotermes is not a reliable indicator of Cretaceous existence since it lives on oceanic islands, probably spread by logs. However its primitiveness [Snyder 1949] is a fairly reliable indicator. Even before the poisonous hard wood and living tissue growing on the periphery of the trunks of angiosperms made its appearance near Korea in the middle of the Cretaceous [Axlerod 1966], the trees showed some evolutionary signs of trunk changes. It may have been an important reason for the large number of pines in wet areas because of their resins and turpentines [Kofoid, 1934]. The sequoias with their very termite chemically resistant wood were to become increasingly dominant well into the Tertiary for their repellent action is more important than toughness [Painter, 1951]. I know of no reports of the effects of Neotermes on present day cycads. This may be because their ranges do not overlap. I can testify that non-native cycads are very susceptible even to Reticulitermes (a soil borne termite) in Texas, however. The Coptotermitinae subfamily of the Rhinotermitidae family from Southeast Asia [Holmgren 1913] may have joined Neotermes in removing the live wood of rain forest toward the close of the Cretaceous and thus help account for the considerable success of angiosperm hardwoods in what remained of the rain forest. A citrus tree, for instance, will rarely die from termites alone even when hollow unless a drought or disease affects it [Hill, 1942].
Even trees which have their living tissue on the periphery eventually may have had difficulty because Mastotermes, the sole surviving species of the primitive Mastotermitidae family, can ring bark trees. It is entirely conceivable that this attribute existed before the close of the Cretaceous because this is, by a wide margin, the most heavily represented family in the Baltic amber (it may have been the typical termite of the eastern North America and Europe) of the early Tertiary and it is not very likely that such an elaborate neural pattern could evolve from a single Australian specie with such a small current population of queens even across the Tertiary. There are 15 fossil known species of Mastotermitidae as opposed to only 8 species of Termitidae [Snyder 1949] even though present day Mastotermes is very ineffective against ants and has only one species. During a raid its soldiers even attack each other and it has no cephalic pore to secrete poison. Mastotermes can eat almost anything derived from plants as well as dead termites. The amber mentioned above might have washed down from a savanna region, however, and ring-barking habits may help account for much of their representation in amber because amber is derived from gum of tree wounds. Mastotermes origin is lost, but its primitive roach like wings hint at a very early existence for its prototypes. Fossil wings have been discovered in the Permian of Kansas which have a close resemblance to wings of Mastotermes, which is the most primitive living termite and which is thought to be the descendant of Cryptocercus genus, the wood roach. This fossil is called Pycnoblattina. It folded its wings in a convex pattern between segments 1a and 2a. Mastotermes is the only living insect that does the same [Tilyard RJ 1937]. Also, mitochondria DNA analysis separates Mastotermes from Kalotermes [Kambhamkati].
I suspect that increased sheet erosion of topsoil was not the only factor affecting the phosphorus economy, or even the most important. Amitermitinae can bore down thousands of centimeters to the water table if necessary [Lee et al 1971, p62]. Fossil termite tunnels have been found in Australia 40 to 50 meters deep [Thiry 2006]. Therefore, not only topsoil is incorporated into the runways. On the contrary, the runways probably consist primarily of materials taken from moist soils in the vicinity of the water table for most species, especially in the driest areas. Their runways are at least suspected of being excavated from lower reaches by Arizona desert termites [Nutting et al 1985, p237]. Evidence of this is that the clay content of the runways is more than double that of the adjacent topsoil. This, even though the topsoil itself is almost certainly derived from previous termite activity since the two species of termites studied are said to be capable of moving soil at an annual rate of 3/4 metric tonnes/ha. Subsoils are notoriously lower in phosphorus than topsoils. Nevertheless, the runways were one third again as high in phosphorus as the adjacent soil. If the runways come from deep down soil, it is therefore highly probable that much of the phosphorus is coming from a secretion of the termites, probably the saliva. The above authors suggest that the approximately four times increase of sodium in the runways over the topsoil is an indication of the use of lower soil profiles. However, the lesser increase of calcium and magnesium makes me suspect that as much as half of the sodium may be coming from the termites drinking the water high in sodium and then excreting the sodium, in effect, with the phosphorus. This is plausible, since something would have to neutralize the phosphate, and for this Gnathamitermes specie studied, potassium could not do it alone. Termites have a saliva which is a little more alkaline than neutral [Hegh 1922, p357].
Other recent analyses of mound material of two Amitermes from northeastern Australia have reinforced the contention that phosphorus is high in Amitermes runways. The increase of total phosphorus in the mounds over the soil was not very great. It ranged from about 10% to about 100% with a rather large standard deviation. The acid extractable phosphorus differed markedly, however. It ranged from two times increase to over ten times. This would seem to indicate that the plants had extracted as much phosphorus as they could from the topsoil analyzed. The increase then would be largely from a secretion of the termites. If the mound soil had been taken largely from the subsoil, much of the insoluble phosphorus would presumably be from the termites as well, and the contribution of the termites would be possibly overwhelming. However, a fairly uniform sodium content in every case casts doubt on this. The phosphorus content of these soils is very low. They are all under 200 parts per million [Okello-Olaya, 1985]. That is probably the reason the termites are not able to raise the total runway phosphorus much. It is obvious that a stage in fertility could be reached from which it would be difficult to lose any more.
For additional analyses bearing on phosphorus in termite earth also see [Wood, 1978] and [Lopez-Hernandez, 1989].
Plants can not live at all below about two parts per ten million of phosphate in soil solution. There is a drop in percentage of phosphorus in plant tissue as phosphorus rises in extremely deficient solution at first. This is because productivity of carbon synthesis rises more rapidly than phosphorus content at first. After about five parts per ten million of phosphate in the soil solution the percentage of phosphate in the plant's tissue then rises with soil phosphorus up to about thirty parts per ten million in soil solution at which point plant phosphorus starts to level off [partly from Pierre, 1953]. The absorption is not influenced by other ions [Bechenbach, 1938] except nitrate ion [Pierre, 1953, p7]. Therefore, any indications of a phosphorus deficiency in plants were probably from the element itself. In the real world the situation is even more severe for the herbivores because there is probably a tendency for plant species with a low genetic need for tissue concentration to become dominant in low phosphorus areas [Orr, 1929 p48, 140].
If large herbivores are present we can be sure that the land is productive and fertile. If only small animals are present we can not be sure that this is because starvation is a main limiting factor or that edible vegetation is present only in small increments, but it is a strong indication. A predominance of fruit and nut eating animals would be a suspicion of a phosphorus deficiency because fruit and nuts do not change much in phosphorus concentration within a species [Turk, 953].
DISCUSSION
An analysis of the runways built on the timbers under a barn located on a mesquite savanna in south Texas by a Reticulitermes of the Rhinotermitidae family for available phosphorus by the agricultural laboratories of Texas A&M; University shows 10 PPM of phosphorus. The adjacent topsoil, a fine sandy soil, has an available phosphorus content of 1 PPM, while the subsoil, which is high in clay and starts about 30 cm down, has 1 PPM. This makes the runways 10 times as high as the topsoil. I can not rule out the possibility that the termites are reaching ancient buried clay strata from an ancient bayou high in phosphorous, which could exist in Aransas County, Texas where these runways were made. It is obvious that the material for the runways is coming from the subsoil or deeper down because the analysis for the runways showed an available PPM for potassium of 117, calcium 351, magnesium 73, copper 0.07 and sodium 35. The corresponding values for the subsoil were potassium 6, calcium 215 magnesium 54, copper 0.01, and sodium 33. These match the runways fairly closely if we can assume that a large proportion of the potassium present is excreted or secreted into the runways. The topsoil had contents, which were potassium 366, calcium 1401, magnesium 888, copper 0.59, and sodium 495. The topsoil values virtually rule out topsoil as a principal source for the runways. The small disparities from the subsoil make it appear as if the soil is not taken from the upper levels of the subsoil either. The higher 5.6 pH of the runways than the 4.6 pH of the subsoil while the topsoil measured 6.0 would tend to corroborate such a source, again assuming that much of the potassium came from the termites. Nitrogen was 1 PPM and sulfur 14 PPM for all. This area is a Mesquite savanna about 5 kilometers inland from the Gulf of Mexico with usually a fairly low but very variable rainfall.
It would be instructive to analyze strata known to be upper Cretaceous soils.
On the Atlantic Highlands of Monmouth County, New Jersey there are red and yellow medium sands which are thought to be delta deposits of an ancient upper Cretaceous Hudson river. They are the Red Bank and Tinton sands formation strata, which were laid down at the same time as the Midwest Lance formation. It is the last strata in which dinosaurs other than birds are found.
On the Raritan Bay side of the hill there was a sheer cliff exposing a series of cross bedded thin plates of iron cemented sand, which may be old soil profiles fossilized by iron solutions draining down from overlying podzolized depositions of flood borne sand. Ramifying throughout this area are what appear to be iron fossilized hollow tubes filled with white sand or clay. I interpret this as roots hollowed out by termites and then filled with sand from the adjoining A horizon of a podzol soil (a soil from the surface of which plant acids have leached iron) by the termites to keep the opening from collapsing in. Humus eating type termites do most of their burrowing in the topsoil [Lee, et al 1971, p52] where the food is most plentiful. If the isoelectric point for iron colloids rose up in elevation in the soil after that, it is conceivable that the sand filled tubes could remain white, and obviously they have remained white regardless of what their origin. One section of a vertical tube revealed its presence by a difference of composition rather than fossilization, which was lighter than the surrounding brilliantly yellow sand. None of the tubes were larger than about 3 cm and were usually about 1.5 cm. Termites don't usually make such large boroughs through soil so I suspect that these were hollowed out tree roots.
At this location there were what appeared to be cavities. They were about 3 cm high and about 30 cm wide. These also were filled with white sands and clays containing a small amount of mica. There were no obvious tubes entering from the side away from the cliff. If these were collapsed below ground termite nests, the white sand could have entered the same way which I suggested for the tubes by other species removing supporting organic construction material from dead termite nests. Apparently it happens that way in today's world [Lee et al 1971, p160].
A few meters down at the bottom of the cliff there was debris of iron cemented sand concretions. One largely intact concretion shaped like a blunt cone about 9 cm wide by about 10 cm high with walls about 1 cm thick was brought back for analysis. It also contained fine white sand containing a few mica grains. Some of the sand grains in the concretion were as large as fine gravel so they must have been the result of some animal transporting them there.
The picture below shows it looking in what I assume is the top;
The picture below shows that nest looking in what I assume is the bottom;
Nasutitermes exitiosus uses grains as large as 2.5 mm [Sleeman 1972][Joachim 1940]. That dimension is close to the fine gravel of this concretion. Nye believes that termites can carry particles as large as 4 mm [Nye]. If so, this concretion is very likely to be from termite action since the surrounding sand had very few such particles. This concretion bears a resemblance to the nest of Eutermes longipennis as described by Hill [Hill 1942] except for a smaller size. This species builds a nest that is a hard shell made of sand and filled with a soft earthy, papery, or woody material. The shape is conical with a blunt or rounded top about 40 cm in diameter and about 50 cm in height. They locate themselves on open, well-drained grassland, scrub or open forest or sandy rises near the margin of plains subject to inundation. Their food is sound and rotten wood, grass and dung.
The analysis was performed on the solution extracted by boiling in aqua regia using the 1955 AOAC method in the State Chemist's Office at Rutgers University. The white sand contained no detectable phosphorus at all. If this was derived from a podzolized A horizon, most of the phosphorus of that soil must have resided in the live plants and litter. The yellow sand contained 0.008% of total phosphorus. The concretion contained 0.13% of total phosphorus. The difference can not be ascribed to the difference in sand content alone because the acid soluble fraction, which is probably largely iron oxides, of the yellow sand was 6.5% and was 35.5% of the concretion.
A second concretion was about 6 centimeters high. The picture below shows a side view, and still containing the white sand;
CONCLUSIONS
If further analyses continue to reveal that Amitermitinae runways are enriched with phosphorus relative to their source, it will make it very plausible that the termites were responsible for the rather drastic changes in bone mass, body size, and loss of teeth during the Cretaceous. The drop in sea level toward the close of the Cretaceous undoubtedly permitted many potent termite genera to migrate around the world. The effects on the biota could have been devastating, and I suspect it is the main reason why the Paleocene was left with an extremely impoverished vertebrate fauna. Animals like termites which have flying reproductives that can fly 3 km or even more with a favorable wind should be able to spread much faster than the seed plants which dominated upper Cretaceous and even more so than plants with vegetative propagation. Even the nomadic Dorylene ants would not be able to keep up with the rain forest termites since Dorylenes reproduce by splitting the colonies, and can not spread across rivers, lakes, or narrow deserts or rock formations. Thus the termites could have a devastating effect on fertility and endemic plants before what few ineffective checks termites had then could catch up with them, even possibly in the rain forests.
Of the dinosaurs only the birds survived, but without teeth. Since birds are usually a predator, the only way that I can conceive of completely losing so valuable an organ as a set of teeth from all non marine species, would be that they went through a period when the young were all insectivorous and were forced to eat termite flying reproductive alates at a time when a high proportion of the alates were humus eaters and therefore had soil in their gut. Evolution toward lightness is not a plausible explanation by itself since gizzard stones are also heavy and lightweight was canceled partly or wholly by stone ingestion. Besides, teeth were retained for tens of millions of years prior to this. The iron and aluminum oxides of tropical soils form a phosphate that is highly insoluble in the slightly acid gut of birds. The Pterosaurs, which also lost teeth, may have been similarly affected. Only the termite species, which specialize in eating humus, pass more than incidental soil through the digestive tract [Lee, 1971 p27]. Therefore if this happened that way, I suspect it would have had to have happened before mid Cretaceous before Nasutitermes and other types capable of utilizing surface detritus had evolved, for after that there would have been little litter for humus formation. It also would have had to have happened in the tropics, so toothed fossils of birds may yet be found in the Arctic or Antarctic. Heat loss is a serious problem for small animals in dry areas, where it can get cold at night. So down and feathers probably evolved for heat conservation at first. Troodontid dinosaurs probably tucked their heads under their limbs when sleeping like modern birds do, probably for heat conservation [Xu]. So birds should have been able to survive in higher latitudes than other dinosaurs. Marine birds retained teeth until the last of the Cretaceous when they were probably supplanted by tropical land based birds that became marine.
REFERENCES for the above article may be seen in the end of Paleocene and Modern Termites.
Back to "Effect of Termites on Phosphorus in the Jurassic"
back to "Did the Permian Wood Roach cause Aridity, Red Beds, and Conifer Rise?"
Back to "Permian Phosphorites from Dragonflies and Amphibians"
See this article for speculation as to what causes silica loss as by alkaline guts of termites
This site shows very good photographs of all the termite families.
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