First published online May 8, 2007
Journal of Experimental Biology 210, 1673-1686 (2007)
Published by The Company of Biologists 2007
doi: 10.1242/jeb.02718
Tribute to P. L. Lutz: respiratory ecophysiology of coral-reef teleosts
Göran E. Nilsson1,*,
Jean-Paul A. Hobbs2 and
Sara Östlund-Nilsson3
1 Department of Molecular Biosciences, University of Oslo, N-0316 Oslo,
Norway
2 ARC Centre of Excellence for Coral Reef Studies and School of Marine and
Tropical Biology, James Cook University, Townsville, Australia
3 National Library of Norway, Oslo, Norway
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Fig. 1. Coral reef at Lizard Island, Great Barrier Reef, Australia. This picture
depicts daytime behaviour of damsefishes (here mainly represented by the
genera Pomacentrus and Chromis) hovering above a colony of
Acropora nasuta. At night, these fishes shelter between branches in
the coral, a microhabitat that can be severely hypoxic. Photo by G. E.
Nilsson.
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Fig. 2. Coral colonies can be severely hypoxic habitats at night. The graphs show
the oxygen levels (A) outside and (B) between branches of Acropora
nasuta colonies from dusk to dawn. Values are means ± s.e.m. from
six measurements on three corals in an outdoor tank at Lizard Island Research
Station. Sunset and sunrise are indicated by broken lines. From Nilsson et al.
(Nilsson et al., 2004 ).
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Fig. 3. Sleep swimming in the damselfish Dascyllus marginatus measured by
video filming them in infrared light on a coral reef in Eilat, Red Sea. The
stroke frequencies of the dorsal, pectoral and caudal fins are about doubled
at night when the fish hide inside coral (Stylophora pistillata)
compared to the `normal swimming' performed outside the coral during the day.
From Goldshmid et al. (Goldshmid et al.,
2004). Reproduced with permission from Limnology and
Oceanography.
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Fig. 4. (A) Fishes (Chromis viridis) sheltering in the hypoxic water
inside a coral colony (Acropora sp.) on the Lizard Island reef at
night during low tide. Oxygen levels between the coral branches varied between
12 and 20% of air saturation. (B) A predatory rockcod (Epinephelus
spilotoceps) lies outside the coral and provides a good reason for the
smaller fishes to use the coral as nocturnal shelter. Photo G. E. Nilsson.
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Fig. 5. Obligate coral dwellers represented by Gobiodon axillaris (A,
left, B), Paragobiodon xanthosomus (A, middle), Caracanthus
unipinna (A, right), and Gobiodon histrio (C). These fishes
spend virtually their whole life between branches of coral, and show a high
degree of hypoxia tolerance. Moreover, G. axillaris, G. histrio and
C. unipinna have excellent abilities for air breathing, apparently
through their scaleless skin. Air breathing is needed if their coral home
becomes air exposed. C shows G. histrio in a coral colony that has
become air exposed during a nocturnal low tide at the Lizard Island reef.
Photos by G. E. Nilsson.
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Fig. 6. A female (A, left) and male (A, right) of the cardinalfish Apogon
leptacanthus. The male is mouthbrooding, as revealed by its expanded
lower jaw. The egg mass of this species makes up about 14% of the body mass of
the male, and constitutes a considerable respiratory obstacle. (B) A male of
Apogon fragilis spitting his brood when exposed to hypoxia in a
closed respirometer, thereby significantly increasing his ability to take up
oxygen. Photos by G. E. Nilsson.
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Fig. 7. Coral-reef fish larvae need to make a transition from top swimming
performance to hypoxia tolerance when they settle on a reef. Relationship
between body mass and (A) oxygen consumption at maximal swimming speed, and
(B) hypoxia tolerance (measured as [O2]crit) in larvae
and juveniles of Chromis atripectoralis. Note the transient drop in
maximum oxygen uptake and simultaneous increase in hypoxia tolerance (seen as
a drop in [O2]crit) that occur when the larvae settle on
the reef and become post-settlement juveniles. Data from Nilsson et al.
(Nilsson et al., 2007b).
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Fig. 8. Transient fall in maximum sustained swimming speed
(Ucrit) when post-settlement size is reached in two
species of damselfish, Amphiprion melanopus (A) and Pomacentrus
ambionensis (B). The fishes were reared in the laboratory and tested in a
swimming flume. From Bellwood and Fisher
(Bellwood and Fisher, 2001).
Reproduced with permission from Marine Ecology Progress Series.
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Fig. 9. Relationship between body mass and (A) hypoxia tolerance (critical oxygen
concentration), and (B) metabolic rate (routine oxygen consumption) in
juvenile and adult coral-reef fishes (excluding pre-settlement larvae). Note
that while hypoxia tolerance does not change with body mass, metabolic rate
shows the `classical' scaling relationship with body mass. The dataset
includes 174 individuals weighing between 40 mg and 40 g and representing 35
species from six families, and is largely the same as that presented in
Table 1 [mostly from Nilsson
and Östlund-Nilsson (Nilsson and
Östlund-Nilsson, 2004), with additional individuals from
Östlund-Nilsson and Nilsson
(Östlund-Nilsson and Nilsson,
2004) and Nilsson et al.
(Nilsson et al., 2007b)]. For
the whole dataset, the mass-specific metabolic rate was related to
mass–0.367 (which translates into a scaling exponent of
1–0.367=0.633 for absolute metabolic rate; r=0.80). For the
best represented family, Pomacentridae with 99 individuals from 14 species,
the same scaling exponents were –0.347 (mass-specific metabolic rate)
and 0.653 (absolute metabolic rate) (r=0.94). Temperature was
28–30°C.
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© The Company of Biologists Ltd 2007
