The results of our study (Rowe et al., 2013) demonstrated a functionally significant relationship between heat storage and submaximal exercise in Asian elephants (Elephas maximus), which was sensitive to seasonal variations in radiant environmental heat. In addition, we modeled behavioral regulation (switching from diurnal to nocturnal activity) of heat storage during prolonged activity (seasonal migrations) in elephants and presumably endothermic polar hadrosaurs (Edmontosaurus). Furthermore, based on post-exercise behavioral observations, we discussed the importance of access to water for increased heat loss in a hot environment.

Gregory Paul expressed two general concerns. Firstly, he questioned the existence of seasonal migrations of distances greater than 1000 km, particularly in polar dinosaurs. Secondly, he questioned the use of captive Asian elephants (forest elephants) to model the thermoregulatory constraints on diurnal activity in full sun. In addition, he suggested that desert-dwelling African elephants (Loxodonta africana) might be (physiologically) adapted for activity in full sun and therefore not subject to the thermoregulatory constraints on activity that we proposed in gigantic species.

Fossil evidence indicates that hadrosaurs were widely distributed in North America at low and high latitudes. Gregory Paul is correct in pointing out the evidence that high latitude populations may have been permanent polar residents (Bell and Snively, 2008; Chinsamy et al., 2012). However, it is likely that large ectothermic dinosaurs would succumb to a lethal level of hypothermia during exposure to several months of cold and dark polar winters (McNab and Auffenberg, 1976; Spotila et al., 1973). Therefore, while our model did not prove endothermic metabolism in hadrosaurs, permanent residency at high latitudes strengthens our argument for endothermic metabolism in polar hadrosaurs.

Furthermore, the absence of adult hadrosaurs in the fossil record, and the presence of juvenile polar hadrosaurs that were too small to escape from late spring flooding, provides evidence that at times adult polar dinosaurs were likely required to walk long distances to escape from catastrophic environmental events. We did not model heat storage in endothermic hadrosaurs during activity in cool environments. However, it is likely that our heat storage model in Asian elephants during the cool seasons – November and February trials at mean air temperatures of 13.7±3.4 and 16.2±4.0°C, respectively – are suitable models for adult endothermic hadrosaurs fleeing from spring floods.

Indeed, our models indicate that in cool conditions adult hadrosaurs could have walked approximately 21–36 km away from rising flood waters before the onset of a lethal core body temperature.

Gregory Paul is likely correct in assuming thermoregulatory variations between active Asian (forest) and African (savannah) elephants. However, heat storage during activity is a function of small surface area to body mass ratio, the rate of metabolic heat production and radiant environmental heat. Active metabolic heat production is similar in Asian and African elephants (Langman et al., 2012). The strength of our heat storage model is measured rates of active metabolic heat production (Langman et al., 2012) in the same Asian elephants we used in our study (Rowe et al., 2013). In addition, exercise trials were conducted before 10:00 h or after 17:20 h CDT, which is similar to the diurnal activity patterns in elephants (Ngene et al., 2009), including desert-dwelling elephants of the Skeleton Coast (Leggett, 2009; Leggett, 2010).

Indeed, desert-dwelling elephants of the Skeleton Coast are presented with thermoregulatory challenges, primarily exposure to direct solar radiation. Gregory Paul suggests that these challenges might be met by unique physiological adaptations that allow desert-dwelling elephants to remain active during high daytime heat loads.

Because palatable vegetation is frequently located at long distances from water sources, desert-dwelling elephants often walk longer distances than other African elephant populations (Leggett, 2009). Gregory Paul reports daily walks in desert-dwelling elephants of greater than 100 km in full sun (Viljoen, 1992; Bartlett and Bartlett, 1992) (see reference to personal communication from D. Bartlett). However, Bartlett and Bartlett (Bartlett and Bartlett, 1992) actually reported daily walks of up to 72.4 km and did not specify whether these movements were recorded during diurnal or nocturnal activity. A 72.4 km walk over 12 h could be performed at approximately 1.6 m s−1, the same average walking speed recorded in African elephants during seasonal migrations of approximately 95 km (Ngene et al., 2009) and similar to the range of walking speed, from approximately 1 to 1.5 m s−1, that minimized the energetic cost of locomotion in elephants (Langman et al., 2012). Furthermore, in the hot dry season, desert-dwelling elephants switched from diurnal to nocturnal walking activity (Leggett, 2010) and night-time ambient air temperatures can drop to approximately 7–10°C, well below the range of ambient air temperatures that reduced a potential lethal level of heat storage in active elephants (Rowe et al., 2013).

Gregory Paul also suggested that desert-dwelling elephants can go without water for days. Seasonal changes in the availability of water determine the movement and activity in desert-dwelling elephants (Leggett, 2009). The ephemeral Hoanib and Hoarusib River basins traverse the Skeleton Coast from east to west and serve as linear oases, where water is usually available throughout the year at spatially separated locations (Leggett, 2006). Contrary to common belief, desert-dwelling elephants spend a greater portion, approximately 10%, of their daily activity budget at water sources compared with other African elephant populations in Tanzania, Uganda and Zimbabwe, which spend approximately 3–5% of their daily activity budget at water sources (Leggett, 2009). In addition, as recorded in other elephant populations (Moss, 1988), at ambient air temperatures greater than 40°C, in the absence of standing water, adult desert-dwelling elephants use their trunks to extract water from their pharyngeal pouch and spray it over their back and ears (Leggett, 2004). Similarly, juvenile elephants used urine-soaked sand to perform the same behavior (Leggett, 2004). The appearance of going without water for days is likely an artifact of behavioral observation sample interval and not a unique physiological adaptation in desert-dwelling elephants. Therefore, rather than uniquely physiologically adapted for survival in a hyperthermal environment, desert-dwelling elephants likely utilize the same behavioral choices described in our study (Rowe et al., 2013) to meet the thermoregulatory challenges of activity in a hot environment.

References

Bartlett
D.
,
Bartlett
J.
(
1992
).
Africa's Skeleton Coast
.
Natl. Geog.
181
,
54
-
85
.
Bell
P
,
Snively
E.
(
2011
).
Polar dinosaurs on parade: a review of dinosaur migration
.
J. Paleo.
32
,
271
-
284
.
Chinsamy
A.
,
Thomas
D.
,
Tumarkan-Deratzian
A.
,
Fiorillo
A.
(
2012
).
Hadrosaurs were perennial polar residents
.
Anat. Rec.
295
,
610
-
614
.
Langman
V. A.
,
Rowe
M. F.
,
Roberts
T. J.
,
Langman
N. V.
,
Taylor
C. R.
(
2012
).
Minimum cost of transport in Asian elephants: do we really need a bigger elephant?
J. Exp. Bio.
215
,
1509
-
1514
.
Leggett
K. E. A.
(
2004
).
Coprophagy and unusual thermoregulatory behavior in desert-dwelling elephants of northwestern Namibia
.
Pachy
.
36
,
113
-
115
.
Leggett
K. E. A.
(
2006
).
Home range and seasonal movements of elephants in the Kuene Region northwest Namibia
.
Afr. J. Ecol.
41
,
17
-
36
.
Leggett
K. E. A.
(
2009
).
Diurnal activities of the desert-dwelling elephants in northwest Namibia
.
Pachy
.
45
,
20
-
33
.
Leggett
K. E. A.
(
2010
).
Daily and hourly movements of male desert-dwelling elephants
.
Afr. J. Ecol.
48
,
197
-
205
.
McNab
B. K.
,
Auffenberg
W.
(
1976
).
The effect of large body size on the temperature regulation of the Komodo dragon, Varanus komodoensis
.
Comp. Biochem. Physiol.
554A
,
345
-
569
.
Moss
C.
(
1988
).
Elephant Memories: Thirteen Years in the Life of an Elephant Family
, pp.
336
.
New York
:
William Morrow and Co. Inc.
Ngene
S. M.
,
Van Gils
H.
,
Van Wieren
S. E.
,
Rasmussen
H.
,
Skidmore
A. K.
,
Prins
H.
,
Toxopeus
A. G.
,
Omondi
P.
,
Douglas-Hamilton
I.
(
2009
).
The range patterns of elephants in Marsabit protected area, Kenya: the use of satellite- linked GPS collars
.
Afr. J. Ecol.
48
,
386
-
400
.
Rowe
M. F.
,
Bakken
G. S.
,
Ratliff
J. J.
,
Langman
V. A.
(
2013
).
Heat storage in Asian elephants during submaximal exercise: behavioral regulation of thermoregulatory constraints on activity in endothermic gigantotherms
.
J. Exp. Bio.
216
,
1774
-
1785
.
Spotila
J. R.
,
Lommen
P. W.
,
Bakken
G. S.
,
Gates
D. M.
(
1973
).
A mathematical model for body temperatures of large reptiles: implications for dinosaur ecology
.
Am. Nat.
107
,
391
-
403
.