**4. Haloarchaea and their relation to avian plumage colour: the case of marine birds**

Studies in the early nineties of the last century demonstrated that the carotenoids of the feathers were derived from the diet and deposited within tissues selectively [53] being the liver one of the most important organs involved in the conversion of carotenoids uptaken [54]. Some years before, other studies focused on seaside birds as flamingos stated that the major carotenoids in blood and feathers were canthaxanthin and a rare β-carotene derivative (4-keto-α-carotene) [55, 56]. Limitations on

chemical and analytical techniques have contribute to the poor knowledge about carotenoids in birds up to nowadays. Fortunately, new advances in spectrometry and HPLC have made possible a significant improvement in this field of knowledge [41, 57]. Thus, during the last 15 years, several research groups worldwide have characterised the nature (and even the concentrations) of carotenoids in blood and feathers, mainly in finches [58, 59] and parrots [44, 60]. All the reported results show that the most important carotenoids contributing to the red-orange-pink colours in feathers are: canthaxanthin, astaxanthin, zeaxanthin and carotene (including its derivatives). In the case of seaside birds, it has been stated that the main rich carotenoids sources are the small shrimps and algae co-inhabiting the salty environments (*Artemia* and *Dunaliella* species, for instance) (**Figure 2**). Consequently, it is extensively assumed that the major pigments in marine bird's feathers would be those predominating in shrimps and algae (astaxanthin, canthaxanthin and carotene). However, some other studies indicate that in hypersaline habitats the birds do not feed extensively on brine shrimps *Artemia* to avoid salt stress [61]. Therefore, other carotenoid rich sources must be considered as part of the diet of marine birds to explain their pigmentation.

Recent contributions in this field have revealed that there are other important factors contributing to the red-orange-pink colour of the feathers. Between them, it is important to highlight the following: (i) genetics [2]; (ii) variation in carotenoidprotein interactions in bird feathers structures, which produces novel plumage coloration [62] and (iii) the presence of alive red-orange microorganisms on the surface of the feathers [63]. This last factor has recently been reported from flamingos growing up in captivity: viable, red-coloured archaeal strains belonging to the genera *Halococcus* and *Halogeometricum* were isolated from the surface of the plumage [63]. Apart from these viable cells, metagenomics approaches showed that cells belonging to other genera such as *Haloquadratum*, *Haloferax*, *Haloarcula*, *Halorubrum* and *Natronomonas* are also present on the surface of the flamingos' feathers. This kind of haloarchaea can produce significant amounts of bacterioruberin, a carotenoid mainly synthesised by them giving the microbial cells red-orange colours [8, 64, 65]. Besides, the analysis of the flamingo plumage pigments shows that bacterioruberin is not only in the alive microbial cells on the feathers' surface, but also found inside the flamingo feathers structure. This result directly suggests that haloarchaea are also part of the diet of flamingos. Bacterioruberin is responsible for the colour of these extremophilic microorganisms (**Figures 3** and **4**) [8, 65]. It has a primary conjugated isoprenoid chain length of 13 C=C units with no subsidiary conjugation arising from terminal groups, which contain four –OH group functionalities only (**Figure 4**).

This carotenoid is involved in several biological roles in haloarchaea: it protects the cells against the damage produced by high intensities of sun radiation, it provides aid in photoreactivation [66] and it promotes membranes stability [8, 65]. Characterisation of pure bacterioruberin samples revealed that it is more powerful than carotene as antioxidant compound [67, 68]. Due to these facts, bacterioruberin could be used in biotechnology and biomedicine for different purposes [8, 69].

**31**

*Haloarchaea May Contribute to the Colour of Avian Plumage in Marine Ecosystems*

Consequently, haloarchaea in general and their pigments in particular, may contribute to the orange-red colour of the feathers in two ways: (i) pink-red haloarchaea cells on the surface contribute to the pink-red phenotype in flamingos' feathers and (ii) haloarchaeal cells are part of the marine birds' diet (at least flamingos), consequently their carotenoids (mainly bacterioruberin) are ingested,

New advances in the knowledge of animal pigmentation state that not only the pigments (carotenoids, melanin, etc.), but also the microstructure of the feathers as well as external factors, contribute to the final phenotype in terms of coloration. Related to birds, and particularly to seaside birds, it was thought that microalgae and small shrimps were the major sources of carotenoids so far. Nevertheless, recent results revealed that other small microbes such as haloarchaea could contribute significantly to the red-orange colours showed by birds like flamingos. In that sense, bacterioruberin becomes a new pigment to be considered to explain animal colours in marine environments. The potential influence of haloarchaea as an environmental factor determining avian plumage coloration or even protecting the microstructures of feathers against UV radiation must be investigated in further studies. Although bacterioruberin has been very well described, only few studies about its biological implications are available at the time of writing this review. Thus, more efforts must be done to explain basic aspects related to bacterioruberin metabolism and its effects on animal health and animal phenotypes. On the other hand, associations between different haloarchaeal-bird species as well as changes in these associations promoted by environmental conditions or anthropogenic actions are worthy to be analysed into detail. Hypothesis based on potential symbiotic relationship between haloarchaea and seaside birds remains unexplored.

This work was funded by research grant from the University of Alicante (VIGROB-309). The authors would like to thank Francisco Grimalt Salvá and José Antonio Abellán for their helpful discussions about the color of the feathers in

*DOI: http://dx.doi.org/10.5772/intechopen.96414*

metabolised and further assimilated.

**5. Conclusions**

**Acknowledgements**

**Conflict of interest**

genera of the *Fringillidae* family and flamingos.

The authors declare no conflict of interest.

#### **Figure 4.**

*Chemical structure of bacterioruberin. This compound has promising potential uses as antioxidant, antitumoral and immunomodulatory molecule for pharmaceutical and cosmetical formulations [64, 65].*

*Haloarchaea May Contribute to the Colour of Avian Plumage in Marine Ecosystems DOI: http://dx.doi.org/10.5772/intechopen.96414*

Consequently, haloarchaea in general and their pigments in particular, may contribute to the orange-red colour of the feathers in two ways: (i) pink-red haloarchaea cells on the surface contribute to the pink-red phenotype in flamingos' feathers and (ii) haloarchaeal cells are part of the marine birds' diet (at least flamingos), consequently their carotenoids (mainly bacterioruberin) are ingested, metabolised and further assimilated.
