Even marsupials living fast and dying young do not match the pace of life of comparable eutherians, part 1
@chuditch @josefnr @torhek @ethan241 @sea-kangaroo @isaacclarey @chewitt1 @ericwilliams @yayemaster @bsmit @tfrench @chiara_paniccia @apgarm @batworker @patrickhaffner @ken_j_allison @alanmuchlinski @asemerdj @mpmoskwik @guillaumeamirault @enricotosto96 @camilojotage @julianbiol @jorgebrito @sulloar @josev_ge @diegoalmendras @azambolli @douglasriverside
(First, please see https://en.wikipedia.org/wiki/Basal_metabolic_rate. To give readers some idea of what the numbers mean: the average adult human body, when at rest, uses energy at about the same rate - viz. about 80 Watts - as the average laptop computer, when in operation.)
Marsupials are extremely diverse morphologically and ecologically (https://en.wikipedia.org/wiki/Marsupial). However, they tend to lag behind comparable eutherians in pace of life (https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5079228/#:~:text=Marsupials%20generally%20have%20a%20low,of%20equivalently%2Dsized%20placental%20mammals.).
For example, the house mouse (Mus musculus, https://en.wikipedia.org/wiki/House_mouse) and 'marsupial mice' (Sminthopsis, https://en.wikipedia.org/wiki/Dunnart) both have body mass about 20 grams. However, the house mouse, when at rest, uses energy at 0.271 Watts, whereas the corresponding value for 'marsupial mice' is only 0.126 Watts - less than half as much.
We can define pace of life as the overall total rate at which the body of a given species uses energy, relative to body mass. Species with the fastest pace of life have maximal rates of metabolism (resting and active), growth, and reproduction per unit mass (https://www.nature.com/articles/s41559-019-0938-7 and https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3140270/).
We would expect that, all else being equal, species with fast pace of life also live only briefly before senescing. This is in keeping with the idea that 'what burns bright tends not to burn for long'.
A familiar example is the house mouse, in which individuals live for only about two years even if they evade mishap. This species - consistent with the rich resources available to it and the predation it tends to attract - not only metabolises and breeds rapidly but is 'hardwired' to have limited life span (https://en.wikipedia.org/wiki/Maximum_life_span).
If this inverse relationship between pace of life and life span holds true for mammals in general, then it seems reasonable to expect those species renowned for the shortness of their life span to have have particularly rapid metabolism.
Does this apply to marsupials?
Particularly abrupt senescence has been studied in certain genera of marsupials such as Antechinus (https://en.wikipedia.org/wiki/Antechinus) and Phascogale (https://en.wikipedia.org/wiki/Phascogale). This constitutes semelparity (https://en.wikipedia.org/wiki/Semelparity_and_iteroparity).
Males make such intense efforts to reproduce that they seem virtually to commit physiological suicide (https://www.nationalgeographic.com/science/article/why-a-little-mammal-has-so-much-sex-that-it-disintegrates). Their first year of sexual activity is also their last. In Antechinus, most female individuals die after raising only a single litter.
However, see the following information. The values show that, even in the case of these small-bodied, insectivorous marsupials, metabolism is slower than in various comparable mammals - particularly shrews (Soricidae) - living on continents other than Australia.
Values for body mass (in grams) and basal metabolic rate (in Watts) are given by Savage et al. 2004 (https://besjournals.onlinelibrary.wiley.com/doi/10.1111/j.0269-8463.2004.00856.x ). To make sense of any comparisons, one must keep body mass as similar as possible.
MARSUPIALS
Dasyuromorphia: Dasyuridae:
Antechinus flavipes 46.5 g, 0.252 Watts
https://en.wikipedia.org/wiki/Yellow-footed_antechinus
Antechinus stuartii 25.0 g, 0.189 Watts
https://en.wikipedia.org/wiki/Brown_antechinus
Antechinus swainsonii 66.9 g, 0.351 Watts
https://en.wikipedia.org/wiki/Dusky_antechinus
(In general, Antechinus spp. have body mass about 50 grams, life span 2 years in females and 1 year in males, neonatal body mass 0.016 g, weaning at 3-4 months old, sexual maturity at about 10 months, gestation period 1 month, time spent by offspring in the pouch 37-178 days, number of offspring per birth 6-12. Eight species in this genus are semelparous.)
Phascogale tapoatafa 154 g, 0.694 Watts
https://en.wikipedia.org/wiki/Brush-tailed_phascogale
(Phascogale tapoatafa is the largest-bodied mammal on Earth in which males senesce at the end of their first breeding season. Females may survive to breed a second time. Information for this species: body mass female mean 145 g, male mean 199 g; breeding seasonal; gestation period about 30 days; number of mammae 8; number of offspring per birth more than 8; time from birth to weaning about 40 days. Phascogale calura is similar to P. tapoatafa in being semelparous.)
Didelphimorphia: Didelphidae:
Marmosa robinsoni 122 g, 0.547 Watts
https://en.wikipedia.org/wiki/Robinson%27s_mouse_opossum
Monodelphis brevicaudata 91.5 g, 0.366 Watts
https://en.wikipedia.org/wiki/Northern_red-sided_opossum
Monodelphis domestica 104 g, 0.335 Watts
https://en.wikipedia.org/wiki/Gray_short-tailed_opossum
EUTHERIANS
Eulipotyphla: Erinaceidae:
Hylomys suillus 58 g, 0.335 Watts
https://en.wikipedia.org/wiki/Short-tailed_gymnure
Eulipotyphla: Soricidae:
Blarina brevicaudata 21 g, 0.344 Watts
https://en.wikipedia.org/wiki/Northern_short-tailed_shrew
Crocidura flavescens 33.2 g, 0.248 Watts
https://en.wikipedia.org/wiki/Greater_red_musk_shrew
Crocidura olivieri 38.6 g, 0.323 Watts
https://en.wikipedia.org/wiki/African_giant_shrew
Suncus murinus 39.7 g, 0.403 Watts
https://en.wikipedia.org/wiki/Asian_house_shrew
(body mass 30-80 and up to 170 grams, life span 1.5-2.5 years, weaning at age 17-20 days, sexual maturity at 45-60 days, gestation period 27-31 days, offspring per birth 1-8, neonatal body mass 2-2.5 g)
Afrosoricidae: Tenrecidae:
Echinops telfairii 116.4 g, 0.750 Watts
https://en.wikipedia.org/wiki/Lesser_hedgehog_tenrec
Hemicentetes semispinosus 116.4 g, 0.380 Watts
https://en.wikipedia.org/wiki/Lowland_streaked_tenrec
Limnogale mergulus 77.7 g, 0.355 Watts
https://en.wikipedia.org/wiki/Web-footed_tenrec
Nesogale dobsoni 44.6 g, 0.315 Watts
https://en.wikipedia.org/wiki/Dobson%27s_shrew_tenrec
Nesogale talazaci 44.0 g, 0.243 Watts
https://en.wikipedia.org/wiki/Talazac%27s_shrew_tenrec
Macroscelidea: Macroscelididae:
Elephantulus brachyrhynchus 49.9 g, 0.303 Watts
https://en.wikipedia.org/wiki/Short-snouted_elephant_shrew
Elephantulus intufi 46.5 g, 0.290 Watts
https://en.wikipedia.org/wiki/Bushveld_elephant_shrew
Elephantulus myurus 63.0 g, 0.387 Watts
https://en.wikipedia.org/wiki/Eastern_rock_elephant_shrew
Galegeeska rufescens 53.0 g, 0.317 Watts
https://en.wikipedia.org/wiki/Rufous_elephant_shrew
Macroscelides proboscideus 39.0 g, 0.292 Watts
https://en.wikipedia.org/wiki/Macroscelides_proboscideus
Petrosaltator rozeti 49.0 g, 0.288 Watts
https://en.wikipedia.org/wiki/North_African_elephant_shrew
The values given above show that the eutherians - with the partial exception of Tenrecidae - exceed the like-size marsupials in metabolic rates.
(The exception of certain species of Tenrecidae is understandable because these insectivores are somewhat analogous to marsupials in living on an isolated landmass with limited predation, namely Madagascar.)
The number of offspring per birth is greater in Antechinus than in shrews of similar body mass, as one would expect from the sizes of the neonates. (Neonatal body mass is 140-fold less in Antechinus than in Suncus murinus, the largest-bodied of all shrews, despite their similar body masses in adulthood.)
However, this does not mean that Antechinus has a fast pace of life.
Suncus murinus (https://en.wikipedia.org/wiki/Asian_house_shrew) grows faster than Antechinus at all stages: gestation, suckling, and development to full body-size. This shrew grows from conception to sexual maturity four-fold faster than does Antechinus of similar body mass: about 82 days vs about 335 days.
Perusal of the values in Savage et al. (2004), beyond the species chosen above, confirms that shrews in general metabolise more rapidly than do equally small-bodied marsupials. Please consider the following.
- Marsupials of body mass about 10 grams have basal metabolic rate less than 0.1: to be precise, 0.06-0.07. Shrews of similar body mass have basal metabolic rate 0.19 (Blarina), 0.12-0.15 (Crocidura), more than 0.25 (Neomys), or 0.30 (Sorex). These values all exceed 0.1, and several of them are 0.2 or more.
- Marsupials of body mass 20-25 grams have basal metabolic rate 0.13-0.19. No shrew of the same body mass is available, but even shrews of body mass 15-20 grams have basal metabolic rate 0.13-0.33.
- Crocidura spp. (33 g, 0.25; 39 g, 0.32) and Suncus sp. (40 g, 0.40) are unusually large-bodied shrews, and thus best-suited to comparison with Antechinus sp. (46.5 g, 0.25) and Pseudantechinus sp. (https://en.wikipedia.org/wiki/False_antechinus, 43 g, 0.15). This shows that, at body mass about 45 g, the marsupials have basal metabolic rate about 0.2, which is only about half of the value for the shrews. A shrew of body mass less than 35 g attains the basal metabolic rate of Antechinus (or close relative) of body mass about 45 g.
- Marsupials in the genera Ningaui and Planigale have body mass 7-12 grams and basal metabolic rate 0.06-0.09. By contrast in shrews, Crocidura, which has similar body mass, has basal metabolic rate 0.11-0.17. For example, compare Crocidura suaveolens (6.9 g, 0.112) with Planigale tenuirostris (7.1 g, 0.063); this is about a two-fold difference. Or compare Ningaui yvonnae (11.6 g, 0.088) with Crocidura spp. (about 12 g, 0.155); this is a difference of up to two-fold.
These values show that shrews, when at rest, metabolise at least twice as rapidly as do like-size marsupials (including genera without the extremely abrupt senescence seen in Antechinus).
Also note that, although pregnancy in Antechinus is abbreviated as in all marsupials, its gestation period is no shorter than that of Suncus murinus: about 1 month in both cases. This is presumably owing to the slow growth of the embryo before birth in the marsupial. Antechinus weans its offspring about 4.5 months after their conception, whereas the corresponding value for Suncus murinus is a only about 47 days - a difference of nearly three-fold.
In summary:
Certain marsupials are remarkable in having specialised on abrupt turnover of generations - to the point of semelparity. However, this is no indication of fast pace of life compared with like-size, insectivorous eutherians occurring on a continent with an intense predatory regime, such as Africa. Although Antechinus and Phascogale are specialised for a short life span, they do not break the generalisation that marsupials are slower in their pace of life than eutherians comparable in body mass.
Slow pace of life is indeed a remarkably consistent aspect of the biology of marsupials, but far less widely known than their remarkably small body size at birth.
to be continued...