Physiological aspects like heat balance, gas exchange, osmoregulation, and
digestion of the early Permian aquatic temnospondyl
Quantitative modeling of an extinct animal's physiology may lead to a
better understanding of its mode of life, including activity, breathing,
feeding, or habitat preferences. However, this is not an easy task since
crucial soft-tissue organs like gills, lungs, intestines, or other internal
organs are usually not preserved in fossils. Therefore, studies on the
paleophysiology of vertebrates have to rely on osteological correlates of
the skeleton (e.g., Janis and Keller, 2001; Wedel, 2003; Schoch and
Witzmann, 2011; Benson et al., 2012). Complementary to osteological
correlates, the extant phylogenetic bracket can be applied and the fossil
animal is compared with its closest living relatives (Bryant and Russell,
1992; Witmer, 1995, 1998). The present study deals with the physiology of
the long-extinct tetrapod
This study is an attempt to assess certain aspects of the physiology of the
large (more than 1 m adult size) Permian non-dissorophoid temnospondyl
Cladogram of temnospondyls (simplified after Eltink and Langer,
2014) showing the phylogenetic relationships of
The Saar–Nahe Basin in southwestern Germany contains a series of late
Carboniferous to early Permian sediments of successive, usually short-lived
(10–1000 years), intermontane lakes within the Variscan mountain belt and
yielded a large number of fossil vertebrates like bony and cartilaginous
fishes and aquatic tetrapods (Boy, 1994; Schoch, 2014). Whereas Schultze and
Soler-Gijón (2004) proposed that the lakes of the Saar–Nahe Basin were
subject to marine influences, recent geochemical analyses indicate that
these lakes were nonmarine in origin (Fischer et al., 2013).
Skeletal reconstruction with body outline of an adult specimen of
During the Permo-Carboniferous, the Saar–Nahe Basin was located in the
tropical region, about 10
The early Permian atmosphere differed from today's atmosphere
especially by its significantly higher O
To make an estimate of the metabolism of an animal, it is indispensable to
know its body mass. The relationship between body mass and metabolic rate is
described by the power curve (Withers, 1992; Heldmaier and Neuweiler, 2004):
In this study, we use a volumetric model called graphic double integration
(GDI) to estimate the body mass of an adult
Graphic double integration (GDI) of
Since no mounted skeleton of
The estimation of body mass for the
A recent analog for
As a stem group amphibian,
All physiological functions in an animal are temperature dependent, and each
organism has its species-specific thermal optimum at which it attains its
maximum efficiency (Heldmaier and Neuweiler, 2004). In analogy with aquatic
amphibians,
For estimation of the average daily metabolic rate (ADMR), the diel activity
of the
Reconstruction of a small larva of
As outlined above, the extant phylogenetic bracket indicates that
Extant amphibians and lung-breathing fishes fill their lungs by vertical movements of the buccal floor that press air from the buccal cavity into the lungs without involvement of trunk musculature (buccal pump mechanism; Brainerd, 1999). In contrast, extant amphibians (but not fishes) use contraction of the transverse abdominal musculature for exhalation (Brainerd et al., 1993; Brainerd, 1998; Brainerd and Monroy, 1998; Brainerd and Simons, 2000; Simons et al., 2000; Brainerd and Owerkowicz, 2006). The straight, short ribs of extant amphibians play no functional role in lung breathing. In contrast, the lungs of amniotes are ventilated by movements of the rib cage (aspiration pump): action of the trunk muscles expands the thorax, generates negative pressure in the lungs, and air is drawn in (Brainerd, 1999; Brainerd and Owerkowicz, 2006; Brainerd et al., 2016).
The ribs of small and middle-sized
Skull, mandible and hyobranchial apparatus of an adult
As outlined above, it can be assumed that fish-like internal gills were
present in adult
Considering these facts, the presence of larval external gills in
Polypterids (or Cladistia) attain a maximum body length of 40–90 cm and
are regarded as the sister group of all other extant actinopterygians
(Graham, 1997; Bartsch, 2004). Similar to lepidosirenid lungfishes and
tetrapods, polypterids possess paired lungs that originate ventrally from
the pharynx (Lechleuthner et al., 1989; Graham, 1997; Brainerd, 2015).
Dependency on air breathing increases with ontogenetic size in polypterids
but never becomes obligatory in well-aerated water (Babiker, 1984; Graham,
1997). Polypterid lungs are very efficient and enable these fishes to rely
completely on air breathing for O
In summation,
Oxygen is about 30 times less soluble in water than in air, and thus its
availability for respiration is limited for animals that breathe water
(Heldmaier and Neuweiler, 2004). To extract a sufficient quantity of
O
The assumption of the following estimations of O
Lung morphometric data (lung volume, tidal volume, etc.) are available for
Using the lung morphometric data and the partial pressure of oxygen
(
The breathing rate for CO
To our knowledge, no data concerning the surface area of polypterid fishes
are available, but they can be compared to other extant air-breathing fishes.
The value for the
Water balance of the
Most fishes and aquatic extant amphibians use suction during aquatic
feeding. However, suction feeding was likely not possible in adult
The content of the food of
Absorption in the
As described above, the paleoenvironment of
Solute balance of the
In the
Most fishes (including basal actinopterygians like polypterids) and
amphibian larvae are ammonotelic animals, i.e., ammonia (NH
No data concerning the relative amount of ammonia and urea in nitrogen
excretion of polypterids are available. However, in other basal
actinopterygians like
Because
The loss and uptake of Na
Synthesizing data and modeling from many sources. Graphic summary
of the physiological reconstructions of the present study for
Physiology of an animal does not fossilize, and therefore our approach to
reconstructing physiological aspects of
The first step was the estimation of body mass based on a skeletal reconstruction and by graphic double integration (Fig. 8). This laid the foundation for almost all further theoretical estimations, and therefore special care was required in reconstructing the skeleton and the body outline. This step was based mainly on fossil evidence (the preserved skeleton) and to a lesser degree on assumptions based on extant analogs (drawing of body outline and assumption of specific gravity).
The second step was the assessment of SMR
dependent on the estimated body mass. This was completely carried out by
comparison with modern analogs, and there is undoubtedly a large source of
error in the choice of the best metabolic rate: even when body mass is
given, metabolic rate may be variable between different individuals of a
group (as shown in Fig. 3 in Heusner, 1982 for different species of
mammals, for example). Therefore, there are not only multiple sources of error concerning
the estimation of body mass of a fossil tetrapod but also in
assessment of metabolic rate when the mass and the taxon that serves as an
extant analog are given. We started our physiological estimation for the
This is not applicable because there are no data sets/research data that could be deposited. All methods and data on which this study is based on are provided in the text and appendix.
All estimations mentioned in the main text are shown below.
Using Adobe Photoshop CS6, 62 vertical lines were drawn across the lateral outline
of the axial body (i.e., 62 slices through the body), each separated by a
distance of 2 cm (Fig. 3a, b). In the same locations, 62 transverse lines
were drawn across the body outline in dorsal view. The vertical and
transverse lines are perpendicular to each other and represent the vertical
(
Body mass can be calculated from the product of volume and density
It must be emphasized here, however, that this value is an estimate with several sources of errors that can be attributed to potential mistakes in the skeletal reconstruction (due to incompleteness of the fossils, distortion of skeletal elements, incorrect reconstruction of the amount of soft tissue covering the skeleton, or inadequate specific gravity assumed), for example. We estimate that the volume calculation may be incorrect by at most 1 L either way, meaning the mass may have been 6 to 8 kg. This range requires notably thin (for 6 kg) or robust (for 8 kg) reconstructions, to the point that they look unlikely. Hence, 6–8 kg is a conservative range and will be used in the following as the basis for physiological estimations.
Head, trunk, and tail (without fin) are subdivided into 63 elliptical
cylinders of 2 cm length (see Appendix A1). The perimeter
Surface areas of fore- and hind limbs were calculated in the same way; the
surface area of both forelimbs is 239 cm
The surface area of the fin was estimated by fitting 14 rectangles in the
dorsal fin and 13 rectangles in the ventral fin. The area of each rectangle
was calculated, the areas summated and multiplied by 2 (left and right
surface of the fin). This method yielded a surface area of the fin of 389 cm
Thus, the total body surface area of the
The range of body temperatures of
This estimate includes potential error in body mass and error resulting from
uncertainty in the allometric curve for metabolic rate of fishes. Using
6000 and 8000 g ranges of body masses yields a range of 10.1–13.1 kJ h
AMR in fishes is typically 1.6 to 3.8 times the
costs connected with SMR (Boisclair and Sirois,
1993). Therefore, it is assumed here that the active metabolic rate at
20
AMR at 25
It is assumed here that
For these estimations, lung volume
The minute volume
The respiratory quotient (RQ) is defined as the ratio of volume CO
Therefore, we assume
Breathing rate (BR) at SMR
The gill surface area required to supply
The gill SA required for
Therefore, the surface area of gills per gram in the
For raw shark meat, 100 g (data from
The overall energy density of the food of
Absorption in the
The kilograms of food per day that
Water flux
In body fluids, the osmotic concentration
Then the estimation of water flux is as follows:
This means that about 173 g water per day was gained through skin and gills
in the
According to Withers (1992), 100 g of protein yields 1.14 mol ammonia. As
estimated in the digestion model (see Appendix A11),
The authors declare that they have no conflict of interest.
This work arose during the Comparative Physiology seminar that was held in
spring 2015 at the Department of Ecology and Evolutionary Biology, Brown
University, Providence, USA. We thank all the participating students for
many fruitful discussions. Florian Witzmann thanks the Alexander von Humboldt Foundation
(