Of bandicoots, beaks and braininess

(writing in progress)

Bandicoots (e.g. Isoodon, Peroryctes, Perameles, Echymipera) and monotremes (e.g. Tachyglossus, Ornithorhynchus) occur only in Australasia. Most of these species fall within a range of body masses (about 200 grams to 5 kilograms) which has been hard-hit by European arrival in mainland Australia. There has been a holocaust of predation by the introduced red fox (Vulpes vulpes) and feral populations of the domestic cat (Felis catus). However, some species of bandicoots and both Australian species of monotremes have – against the odds – evaded extinction. Since introduced predators seem to outsmart native mammals, the question arises of whether bandicoots and monotremes have survived partly because of unexpected braininess.

An immediate problem with this explanation is that bandicoots and monotremes are extremely different in their braininess. And it is the monotremes – despite all their primitive features - which have surprisingly large brains.
 
Braininess, i.e. brain mass scaled relative to body mass, is measured by the encephalisation quotient (EQ), which by definition is 1.0 in the average mammal. The values for red fox and domestic-gone-feral cat are respectively about 2.0 and 1.0. Nobody should be surprised that these Carnivora are brainier than either bandicoots (EQ 0.4-0.55 in families Peramelidae and Peroryctidae) or monotremes (EQ 0.8- 0.95). But what is surprising is that the values for monotremes – supposedly ‘living fossils’ - so closely approach that of the cat (see Box 3).

Monotremes lay eggs, which is typical of small-brained reptiles rather than large-brained mammals. Echidnas seem somewhat reptilian also in their sluggish movements, limited body temperatures, and beaked mouth lacking any teeth. By contrast, bandicoots seem more advanced than other marsupials in possessing a true allantoic placenta – making them ‘placental marsupials’ despite gestation periods as brief as 12.5 days. Given these facts, bandicoots might be expected to be brainier than monotremes. But the opposite is true.

The short-beaked echidna is a particular surprise in possessing the largest prefrontal cortex, relative to body mass, of any mammal. Since this part of the brain connotes intelligence, such encephalisation in a non-social, apparently relictual mammal with relatively simple behaviour has yet to be explained.

If bandicoots and monotremes are so different in their braininess, how have both groups coped with introduced carnivores?

Although the platypus seems remarkably vigilant when floating, evasion of predators does not seem to involve special intelligence in either monotremes or bandicoots. Instead, the Australian monotremes are protected, while foraging, by an aquatic medium in one species and by dorsal spines in the other. In the case of the short-beaked echidna, a combination of armour and rapid excavation has more than compensated for an inability to run. For their part, bandicoots survive by virtue of rapid reproduction by marsupial standards– although no match for certain eutherians such as the introduced rabbit (Oryctolagus cuniculus). Rather than emphasising maternal care, bandicoots practise ‘easy come, easy go’ reproductively. Mothers sometimes jettison – and thus sacrifice - pouch young when stressed.

Bandicoots are even less brainy than most other marsupials but combine omnivorous opportunism with unusually rapid growth for Australian mammals. Their populations can survive predatory pressure where cover (e.g. thickets of introduced Lantana) is sufficient.

However, none of this explains the anomalous braininess of monotremes. Perhaps some lateral thinking would help?

Birds and mammals have different patterns of scaling of brain size to body size. Although small birds generally exceed like-size small mammals in brain size, large birds have smaller brains than those of like-size mammals even where similar in intelligence. This applies, for example, to a comparison of the platypus with the ecologically similar and like-size musk duck (Biziura lobata) – which falls short by at least one gram of brain tissue despite being the brainiest duck in Australasia. The brains of large birds seem more compact - compensating for inferior quantity by having superior quality - than those of mammals, in keeping with a premium on lightness in flying animals.

In particular, birds lack the substantial prefrontal cortex of mammals but instead use a diminutive but powerful part of the cerebrum called the pallium. The scaling of brain size to body size is such that the brains of the larger birds are efficient in the sense that they achieve comparable intelligence with less brain matter than in mammals (see https://www.theguardian.com/environment/radical-conservation/2016/nov/05/birds-intelligence-tools-crows-parrots-conservation-ethics-chickens ). So, the prefrontal cortices show a particular contrast in platypus vs musk duck.

In acknowledgement of the different equations followed by birds and mammals in the scaling of brain sizes to body sizes, EQ has long been calculated independently for birds and mammals. Avian EQ rates e.g. cockatoos relative to other birds but would underrate avian braininess according to the calibration of EQ in primates. Could a similar but inverse principle possibly apply to the egg-laying mammals?

Based on this line of reasoning, could these two groups of egg-layers, namely birds and monotremes, be opposites in the sense that the former has maximal constraints on brain weight at a given level of intelligence, whereas the latter has minimal constraints? That is to say: could a previously unrealised pattern of scaling mean that monotremes have brains even less compact than those of typical mammals including marsupials?

Heavy brains in monotremes seem consistent with the trend – at least in the few surviving species - of exploiting gravity rather than defying it in the avian way. The platypus is odd in using the same fore feet for burrowing as well as swimming, and its weight aids submergence while foraging in a buoyant medium. The short-beaked echidna puts weight into excavating insects, and is remarkably adept at submerging on-the-spot in solid earth when attacked, rather than tunnelling obliquely as most digging mammals would. Is such vertical sinking not, in a sense, opposite to the lift-off on which birds rely?

Birds have apparently upgraded the hardware in their nervous systems in order to reduce the weight particularly of the cortex, with no loss of intelligence. Evolutionary compaction of the brains of large birds seems consistent with not only aerodynamics but also the speed of neural impulses at the body temperatures of flying birds, which exceed those of mammals. A lesser nervous efficiency in monotremes than in birds of similar body masses seems in line with the extreme differences in body temperatures: about 31 degrees Celsius in monotremes versus 41 degrees Celsius in e.g. cockatoos.

The bulkiness of the brains of monotremes is antithetical to the lightness of brains in the avian counterparts for monkeys in primate-free Australasia. The most intelligent of the larger birds – such as cockatoos and crows - all have brains more compact than those of monkeys of similar body mass on other landmasses, despite rivalling the primates in intelligence. Which surprises await us in future studies comparing the brains of monotremes with both birds and non-monotreme mammals, using histology, neurology and physiology?

Why bandicoots and monotremes are brain-strainers:

Bandicoots seem to be – apart from pigs (Suidae) - the only generalised, omnivorous, non-armoured mammals on Earth which are less than half as brainy as expected for mammals (i.e. EQ less than 0.5). For their part, monotremes seem to be the only non-avian egg-laying vertebrates which approach typical mammals in braininess (EQ exceeding 0.8).

In general within mammals, encephalisation is partly explained by pregnancy: the longer the gestation of the species relative to body size, the larger the brain relative to body size. Viewed this way, the decephalisation of bandicoots loses some of its surprise because they have short gestation even for marsupials. There is a particular contrast with the superficially similar potoroos (Potorous spp.), which lack an allantoic placenta because they are related to kangaroos, but gestate longer - about 38 days - than even the largest species of kangaroo. Sure enough, bandicoots seem decephalised relative to the superficially similar potoroos.

However, this fails to explain the encephalisation of monotremes, which hardly gestate at all. Against expectations, monotremes seem encephalised relative to potoroos.
 
This puzzle is accentuated by metabolic rates and anti-predator defences.
 
Metabolic rates: monotremes have minimal body temperatures for mammals, of about 31 degrees Celsius. In eutherian mammals there is some correlation between basal metabolic rates and brain sizes. Seen in this light, echidnas (Tachyglossus and Zaglossus) are surprisingly brainy for such slow-moving animals. 
Anti-predator defences: both the short-beaked echidna (Tachyglossus aculeatus) and the platypus (Ornithorhynchus anatinus) are unusually defended for Australasian mammals. The former has spiny armour, whereas the latter has a venomous spur on the hind leg. Except for certain porcupines, armoured or venomous mammals tend to be decephalised, with EQ similar to those of bandicoots (which possess no unusual defences). One surprise is that the short-beaked echidna is brainier than most armoured mammals of comparable body size, such as armadillos, tenrecs, hedgehogs and pangolins, all of which are decephalised with EQ less than 0.5. The comparison with pangolins is telling because these primitive mammals, like the short-beaked echidna, specialise on a diet of ants and termites. Indeed, pangolins complement the distribution of echidnas by occurring in Indonesia up to the edge of Australasia. A second surprise is that the platypus is brainier than most venomous mammals such as solenodons, shrews, skunks and tenrecs (see https://en.wikipedia.org/wiki/Venomous_mammal ).

Bandicoots and monotremes lactate as all mammals do, but bear extremely poorly developed offspring after minimal gestation. In the case of bandicoots the newborns are smaller than in comparable eutherians and the gestation periods are shorter than in any eutherian, including mice and shrews far smaller than the bandicoots. In monotremes the offspring emerge at the stage of the egg.

The short-beaked echidna is similar in body mass and diet (mainly termites and beetles) to the bat-eared fox (Otocyon megalotis) of Africa, and the two species have similar brain masses, in the range 25-28.5 grams. For comparison, the brain of the domestic-gone-feral cat weighs about 30 grams while that of the red fox weighs about 49 grams – all having similar body size. Given that the red fox is among the brainiest of Carnivora, and given that the bat-eared fox may need particular wits to survive among African predators, the convergence in brain size between the short-beaked echidna and the most insectivorous of foxes is surprising. Although the braininess of the short-beaked echidna falls far short of that of the red fox, the fact that it approaches that of any species of fox casts doubt on the validity of applying typical mammalian standards to the EQ of monotremes. 

 
The following shows the brain mass of the short-beaked echidna relative to a representative selection of other mammals including bandicoots and other marsupials.

http://ars.els-cdn.com/content/image/1-s2.0-S1095643303001661-gr2.gif

Further background information: https://static-content.springer.com/esm/art%3A10.1186%2Fs12862-014-0178-z/MediaObjects/12862_2014_178_MOESM6_ESM.gif

 
In a previous Post I have discussed the decephalisation of bandicoots. However, what has been lacking is a satisfactory frame of reference.

Here is a comparison of bandicoots with monotremes.
 
Bandicoots and monotremes are both restricted to Australasia including New Guinea.
 
Both bandicoots and monotremes depart from the ‘normal’ mode of reproduction in mammals, by giving birth to ‘premature’ young. In the case of bandicoots the neonates are far smaller than in comparable eutherians, while in monotremes the reproduction is egg-laying.
 
Since egg-laying could be considered more ‘primitive’ than marsupial reproduction, and since bandicoots are more ‘advanced’ than other marsupials in the possession of a true allantoic placenta, it might be expected that the bandicoots would exceed the monotremes in brain size relative to body size.
 
In fact the opposite is true: the brains of the monotremes are almost twice as massive, relative to body mass, as those of the bandicoots.
 
Among mammals generally, a value of 1.0 for EQ means average braininess for a mammal. The values for EQ in monotremes are 0.8-0.95, while those in bandicoots (families Peramelidae and Peroryctidae) are only < 0.5 in some spp. and < 0.6 in all spp.
 
This relationship is surprising not only because of the reproductive modes of the animals, but also because of their rates of metabolism and the modes of anti-predator defence.
 
The short-beaked echidna (Tachyglossus aculeatus) has an extremely low body temperature for a mammal, of about 32 degrees C if memory serves. In eutherian mammals there is a general correlation between basal metabolic rates and brain sizes, which means that, by those standards, this echidna has a disproportionately large brain. 
 
Another reason to be surprised at the relatively large brain of the short-beaked echidna is the fact that this species has a specialised diet of termites and ants. Myrmecophages worldwide tend to have small brains for their body sizes, and this applies to the numbat (Myrmecobius fasciatus), which formerly coexisted with the short-beaked echidna in parts of southern Australia.
 
Both echidnas and the platypus (Ornithorhynchus) are unusually defended for Australasian mammals. The former have spiny armour, whereas the latter has venom delivered by a hind claw. In general, armoured and venomous mammals tend to be decephalised, with EQ values similar to those of bandicoots (which are not unusually defensive). Given their tendency to reliance on special defences, the monotremes are unexpectedly brainy in the context of mammals generally.
 
Extinctions owing to the introduction of the red fox (Vulpes vulpes) and the feral cat (Felis catus) have affected mammals of body mass 1-5 kg particularly severely. The result is that most native mammals of the body masses of bandicoots and the short-beaked echidna have disappeared from the Australian mainland. In the case of the few species of bandicoots that have survived this catastrophe, and the short-beaked echidna, which remains relative widespread and common, it may be asked which adaptations have allowed these species to evade predation.

In neither case is it likely that encephalisation has been important. In the case of bandicoots, reproduction is rapid enough that certain species can survive provided there is enough cover. In the case of the short-beaked echidna, the effective defence seems to be a combination of a spiny back and extremely rapid digging when alarmed.
 
Do large brains necessarily correlate with intelligence?

Firstly, let’s not get bogged down in the definition of intelligence. Let’s just assume that, however we define intelligence, we’re defining it consistently across the board.

Now, as I see it there are at least two ways in which ‘large brains don’t necessarily correlate with intelligence’.

The first is that brain size must be considered relatively to body size, not absolutely. The brain of a hippo is absolutely larger than that of a monkey, but the monkey is by far the more intelligent. This is because brain size can only be expressed as encephalisation after calculating its relationship to body size, using a power function (allometric exponent).

The second is that different classes of animals have different degrees of compactness of brain tissue. Those with extremely compact brain tissue can achieve a given level of intelligence with relatively small brains. The best-documented example of this is the comparison of birds with mammals. Birds seem to achieve ape-like levels of intelligence with brains far smaller than those of apes, relative to body size (according to the allometric exponent). This compactness of the birds’ brains makes sense in terms of minimising weight in animals that need to be light to fly flappingly.

My suggestion that monotremes differ from other mammals in having less compact brains than the other mammals is, as far as I know, an original suggestion. The trouble with testing it is that there are simply too few – indeed far too few – species of monotremes still living on Earth for us to get anything like the required statistics. In the case of the bird-mammal comparison, we have thousands of spp. in our comparison; and even here there are complications. For example, if you look carefully at the allometric regressions for brain size relative to body size in birds vs mammals, you’ll notice that the slopes of the lines differ.

What this means is that, while it is true that in large birds such as cockatoos the brains are smaller than in like-size mammals such as primates, when it comes to small birds such as sparrows and finches it is actually the birds that have the larger brains than those found in like-size mammals such as mice. I.e. in small birds the whole question of compactness seems to fall away, and a sparrow of say 25 grams actually has an absolutely larger brain than a comparably intelligent rodent of 25 grams.

Given such complications and subtleties, there seems little chance that anyone could ‘prove’ my point about monotremes having brains that are even less compact than those of other mammals. This is, of course, not a reason to be silent on this possibility; it is merely to acknowledge that in some cases in science there are significant theoretical possibilities which remain, in some sense, untestable.

Another question raised by my suggestion is whether the degree of compactness (or should I say un-compactness) of monotreme brains is in line with that in reptiles, or not. Do reptiles have brains of similar compactness to those in mammals? If so, do monotremes constitute a category of compactness of brain tissue different from those of both other mammals and reptiles?

(writing in progress)

Publicado el junio 19, 2022 03:39 MAÑANA por milewski