Thesis Project:

                        Exploring possible remodeling of respiratory structures

                         in Gambusia affinis (Baird & Girard, 1853)

           The purpose of my study is to further explore the ability of some fishes to reversibly remodel their gill surface area. In 2003, researchers at the University of Oslo in Norway, discovered that the Crucian carp, Carassius carassius, has the ability to change the surface area of its gills in response to hypoxia (2003). When in normoxic waters the gills of the C. carassius look club-like with much reduced surface area. When exposed to hypoxic waters the gills of C. carassius look like typical fish gills with protruding lamellae and a much greater surface area (Figure 1). This change in morphology is possible due to the presence of a mass of cells (termed the interlamellar cell mass, ILCM) in between their lamellae in normoxic waters (Figure 2). When exposed to hypoxic waters, a combination of increased cellular apoptosis and reduced mitosis diminishes the ILCM.
This ability to change the surface area of their gills is an interesting adaptation for dealing with opposing ionoregulatory and respiratory needs. A greater gill surface area (specifically the lamellar surface area) is beneficial for oxygen uptake, but detrimental for maintenance of blood ion concentrations. Having the ability to change lamellar surface area allows C. carassius to reduce metabolic costs associated with ion regulation when oxygen is readily available and enhance their oxygen uptake when oxygen concentrations drop.
In subsequent years, several new studies have found that more species also have the ability to remodel their gills (Matey et al., 2008; Ong et al., 2007; Sollid et al., 2005b). Two of these species are in the same phylogenetic order, Cypriniformes, as C. carassius. However, one species is in the order Cyprinidontiformes, which is distantly related to the Cypriniformes. Another species Salvelinus fontinalis (Brook trout), when exposed to aluminum, exhibited a reaction which may be similar to the remodeling exhibited by C. carassius (Mueller et al., 1991). As this ability has been further explored, it seems it may not be as unique as was initially thought. Fishes in two distantly related orders seem to have exactly the same mechanism for dealing with the ‘Osmoregulatory Compromise’ (discussed below).
Based on this, my general hypothesis is that this ability is much more widespread than is currently known. To test this hypothesis, I have chosen a species which displays characteristics that may be indicative of an ability to remodel its respiratory surface area. This species was also chosen with the aim that my work will help to begin answering questions about the evolutionary history of gill remodeling (discussed below).
In addition to simply identifying this ability in another species of fish, I also would like to explore the small-scale cellular changes that occur in the gill epithelium and in the ILCM. Matey et al (2008) conducted a detailed study of these changes in the Lake Qinghai scaleless carp, Gymnocypris przewalskii. They found that the structure of different types of cells (specifically Mitochondria Rich Cells) changed as lamellar surface area changed. I would like to compare the cellular structure and changes that occur if Gambusia affinis have the ability to remodel their gills to those found in G. przewalskii. This may give more insight into how similar or dissimilar these changes are in the two different orders of fishes.

Literature Cited
Matey, V., Richards, J. G., Wang, Y., Wood, C. M., Rogers, J., Davies, R., Murray, B. W., Chen, X. Q., Du, J. and Brauner, C. J. (2008). The effect of hypoxia on gill morphology and ionoregulatory status in the Lake Qinghai scaleless carp, Gymnocypris przewalskii. Journal of Experimental Biology 211, 1063-1074.
    Mueller, M. E., Sanchez, D. A., Bergman, H. L., McDonald, D. G., Rhem, R. G. and Wood, C. M. (1991). Nature and time course of acclimation to aluminum in juvenile brook trout (Salvelinus fontinalis). II. Gill histology. Canadian Journal of Fisheries and Aquatic Sciences 48, 2016-2027.
    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. Journal of Experimental Biology 210, 1109-1115.
    Sollid, J., De Angelis, P., Gundersen, K. and Nilsson, G. E. (2003). Hypoxia induces adaptive and reversible gross morphological changes in crucian carp gills. Journal of Experimental Biology 206, 3667-3673.
    Sollid, J., Weber, R. E. and Nilsson, G. E. (2005). Temperature alters the respiratory surface area of crucian carp Carassius carassius and goldfish Carassius auratus. Journal of Experimental Biology 208, 1109-1116.