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First published online October 31, 2008
Journal of Experimental Biology 211, 3519-3521 (2008)
Published by The Company of Biologists 2008
doi: 10.1242/jeb.013599
JEB Classics |
A FIRST LOOK AT HOW FISH GILLS WORK
Universität Bonn
perry{at}uni-bonn.de
|
In respiratory science, many now-famous names in comparative respiratory physiology such as Pierre Dejours, Hans-Rainer Duncker, Kjell Johansen, Johannes Piiper, C. Ladd Prosser, Hermann Rahn, Knut Schmidt-Nielsen, S. Marsh Tenney and Ewald Weibel were well into their careers. Physiological ecology was emerging.
Among the major players was also George M. Hughes. After focusing on
control of respiration and locomotion in invertebrates such as dragonfly
larvae, crabs and marine snails early in his career, Hughes began studying
fish respiration in the late 1950s, and it became his strength over the
following three decades. In addition to numerous reviews, book chapters and a
popular book on comparative respiratory physiology
(Hughes, 1963
), Hughes has
published over 200 peer-reviewed papers, two-thirds of them on fish
respiration. Of these publications three have been cited more than 200 times
(Hughes, 1966;
Hughes, 1972;
Hughes and Morgan, 1973).
In his classic 1966 paper, `The dimensions of fish gills in relation to
their function' (Hughes, 1966),
Hughes founded the modern age of gill biophysics, by measuring various gill
tissue dimensions in fish ranging from 12 g mackerel (Trachurus
trachurus) to 1.5 kg angler fish (Lophius piscatorius), to
analyse gill resistance to water flow. The paper is presented in the IMRD
(introduction, methods, results, discussion) format, typical of experimental
studies, although it is actually an integrative and analytical review of
factors involved in gill resistances supplemented with new morphological
data.
In the Introduction, Hughes focuses on the rationale for the paper, stating
that `The present investigation was undertaken because earlier work
(Hughes and Shelton, 1958)
suggested that the nature of the gill resistance is an important variable in
the ventilation mechanism.' In that paper, Hughes and Shelton had suggested
that the secondary lamellae, the microscopic flap structures on gill filaments
where gas exchange occurs, might be so closely spaced and water so viscous
that water may not penetrate between the lamellae: that is, they may not be
ventilated directly (Fig. 1).
In that case, the diffusing capacity of the gill, which is inversely
proportional to the distance that oxygen must travel by diffusion from the
gill surface to the nearest blood space, would be vastly overestimated by
earlier morphological studies, which had assumed that diffusion begins at the
lamellar surface. If water cannot flow between the lamellae, then the
dimensions of the interlamellar spaces must be added to the total distance
that gas molecules must move on the basis of diffusion alone. But how much of
the interlamellar space must be included? In addition, Hughes doubted that the
pressure differential of 0.5 cm H2O measured across the
gills would be sufficient to overcome the resistance of a fine gill sieve and
ventilate the interlamellar spaces (Hughes,
1985). Hughes realised that a biophysical model that directly
verified fluid flow through the gill would clear up these doubts.
|
) and further
refined by Hughes to measure various gill morphology parameters, including
filament length, secondary lamellae spacing and surface area. Many of these
methods were later to become standard in gill morphometry. The technique for
secondary lamellar surface area measurement was particularly laborious and it
is perhaps fortunate that modern methods for measuring gill surface area
(Costa et al., 2007) did not
exist in 1954 and 1966, otherwise the parameters necessary to construct the
biophysical model, such as filament number and length, and secondary lamellar
height, length and frequency, might not have been measured.
In the Results section, Hughes reviewed gill parameters in the context of
fish lifestyle while also analysing the biophysical implications of secondary
lamellar dimensions and interlamellar distance for ventilation. To this end
Hughes employed a modified version of the Poiseuille equation to calculate
flows through a rectangular aperture and estimate the resistance to fluid
flowing between secondary lamellae. He came to two conclusions. First, the
gill surface area correlates with lifestyle in marine fishes, as Gray had
already stated (Gray, 1954), as
well as for hemoglobin-free icefish (Chaenocephalus sp.) and two
fresh-water species; the sea trout (Salmo trutta) and the tench
(Tinca tinca). Second, not only was the mesh of the gill sieve formed
by the interlamellar spaces calculated to be large enough to allow direct
ventilation, but also the maximum calculated ventilatory rate based on the
morphometric data was an order of magnitude greater than that measured
physiologically. Taking a closer look at different anatomical variables, such
as increasing gill surface area by increasing the mean length of filaments
(thereby increasing the number of secondary lamellae) or by increasing mean
lamellar height, resulted in an increase both in gill surface area and in
water flow over the surface. However, Hughes also calculated that increasing
the area by increasing the mean lamellar length, or decreasing the
interlamellar distance, would be accompanied by a large decrease in water flow
across the respiratory surfaces.
The Results section merges imperceptibly with the Discussion, in which Hughes discusses the tradeoffs in gill structure and function and identifies and analyses dead space (i.e. the water volume that lies outside the interlamellar spaces), as well as illustrating how the fish might actively control the use of dead space. Particularly interesting is the implication of the possibilities of blood movement within the filaments. Most of the blood flows through the secondary lamellae, returns through efferent filamentar arteries to the gill arch and is distributed then to the body (Fig. 1). In 1966 alternative pathways of blood flow within the filaments had just been recognised by other researchers but the significance was not clear. Hughes suggested that the mechanisms for controlling the flow of blood to these other vessels (central venous sinus and branchial vein; Fig. 1) within the filament might be under humoral and nervous control, just like pulmonary blood flow in the mammalian lung. The significance of this albeit speculative statement should not be underestimated, as it highlights the importance of comparative studies in the recognition of overarching principles. Such observations, which can only be made by a person with broad experience, ranging from the molecular level right up to the whole animal in its environment, can stimulate basic research for generations to come.
During the course of this study, Hughes was meticulous in his measurements. For example, gill structure is not uniform; most teleost fish have four pairs of functional gill arches that are bilaterally symmetrical but differ from anterior to posterior. Also, the filaments within a given arch have different lengths and the structure of the secondary lamellae differs along the length of the filament. In order to take into account all of these deviations from uniform structure, Hughes took samples from the base, middle and tip of every tenth filament in all arches from one side of the fish, and fixed the tissue in Bouin's solution before transferring it to 70% ethanol and measuring the dimensions of the filaments and lamellae. Based on his experiences, Hughes was able to simplify the procedure later, by taking only the second arch on one side of the fish and multiplying by eight to represent the whole gill apparatus in subsequent publications. To measure the secondary lamellar surface area, Hughes dissected individual or pairs of secondary lamellae, traced them onto graph paper using a camera lucida and determined the surface area of these projections by point counting. In addition, he determined the number of secondary lamellae per millimeter of filament (secondary lamellar frequency). From all this information it was possible to reproducibly give an estimate of gill surface area.
However, even if measurements are reproducible it does not necessarily mean
that they are correct, and not all of Hughes' assumptions have stood the test
of time. For example, secondary lamellae are only rarely flat, and the height
of secondary lamellae is related to the oxygen tension in the water (see
Nilsson, 2007;
Ong et al., 2007) and/or
temperature. In addition the surface area of the lamellae is certainly
underestimated by removing them manually: a very demanding procedure that can
only err in the direction of underestimation. Preliminary studies on trout
gills have indicated that the underestimate may be approximately a factor of
two in this species (Höller,
2004). A further limitation of Hughes' method is that it only
applies to fish with secondary lamellae that can be manually removed. Thus
extremely small species or those that lack secondary lamellae (e.g. lungfish
of the genera Protopterus and Lepidosiren) would not be
measurable.
All of this, however, does not change the basic assumptions, models and
conclusions of Hughes' 1966 paper, and that contributes to its timelessness.
The paper's main impact, and the reason it is still cited, is that it is the
first study to apply engineering principles to gills. The paper has been cited
212 times, and continues to be cited regularly as it enters its fifth decade.
The interest in the self-regulatory mechanisms and how gills work continues
(Nilsson, 2007) and Hughes'
paper is where this interest began.
Footnotes
Steven Perry discusses G. M. Hughes' 1966 paper entitled: The dimension of fish gills in relation to their function. A copy of the paper can be obtained from http://jeb.biologists.org/cgi/content/abstract/45/1/177.
References
Costa, O. T. F, Pedretti, A. C. E., Schmitz, A., Perry, S. F., Fernandes, M. N. (2007). Stereological estimation of surface area and barrier thickness of fish gills in vertical sections. J. Microscopy 225,1 -9.[CrossRef][Medline]
Gray, I. E. (1954). Comparative study of the
gill area of marine fishes. Biol. Bull.
107,219
-225.
Höller, S. (2004). Eine neue stereologische Methode zur Bestimmung der Kiemenoberfläche bei Fischen. Diplomarbeit, Universität Bonn.
Hughes, G. M. (1963). Comparative Physiology of Vertebrate Respiration. London: Heinemann.
Hughes, G. M. (1966). The dimension of fish
gills in relation to their function. J. Exp. Biol.
45,177
-195.
Hughes, G. M. (1972). Morphometrics of fish gills. Resp. Physiol. 14, 1-25[CrossRef][Medline]
Hughes, G. M. (1985). This week's citation classic. Hughes, G. M. The dimension of fish gills in relation to their function. Journal of Experimental Biology 45, 177-195, 1966. Curr. Contents 4,16 .
Hughes, G. M. and Morgan, M. (1973). The structure of the fish gills in relation to their respiratory function. Biol. Rev. 48,419 -475.
Hughes, G. M. and Shelton, G. A. (1958). The mechanism of gill ventilation in three freshwater teleosts. J. Exp. Biol. 35,807 -823.[Abstract]
Nilsson, G. E. (2007). Gill remodeling in fish
— a new fashion or an ancient secret? J. Exp.
Biol. 210,2403
-2409.
Ong, K. J., Stevens, E. D. and Wright, P. A.
(2007). Gill morphology of the mangrove killifish
(Kryptolebias marmoratus) is plastic and changes in response to
terrestrial air exposure. J. Exp. Biol.
210,1109
-1115.
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