Embryo oxygenation in pipefish brood pouches: novel insights

Abstract

The pipefish brood pouch presents a unique mode of parental care that enables males to protect, osmoregulate, nourish and oxygenate the developing young. Using a very fine O 2 probe, we assessed the extent to which males of the broad-nosed pipefish (Syngnathus typhle) oxygenate the developing embryos and are able to maintain pouch fluid O 2 levels when brooding in normoxia (100% O 2 saturation) and hypoxia (40% O 2 saturation) for 24 days. In both treatments, pouch fluid O 2 saturation levels were lower compared with the surrounding water and decreased throughout the brooding period, reflecting greater offspring demand for O 2 during development and/or decreasing paternal ability to provide O 2 to the embryos. Male condition (hepatosomatic index) was negatively affected by hypoxia. Larger males had higher pouch fluid O 2 saturation levels compared with smaller males, and levels were higher in the bottom section of the pouch compared with other sections. Embryo size was positively correlated with O 2 availability, irrespective of their position in the pouch. Two important conclusions can be drawn from our findings. First, our results highlight a potential limitation to brooding within the pouch and dismiss the notion of closed brood pouches as welloxygenated structures promoting the evolution of larger eggs in syngnathids. Second, we provide direct evidence that paternal care improves with male size in this species. This finding offers an explanation for the documented strong female preference for larger partners because, in terms of oxygenation, the brood pouch can restrict embryo growth.

Evolutionary ecology of pipefish brooding structures: embryo survival and growth do not improve with a pouch

“…These results are in line with recent measurements that showed that, in S. typhle, oxygen levels within the pouch were substantially lower than in the surrounding waters, both in normoxia and in hypoxia (Braga Goncalves et al. 2015a). In terms of behavior, we found that ventilation rates and proportion of time spent in the top half of the water column increased significantly in hypoxia (discussed below in relation to the brood pouch).…”

“…2002; Stölting and Wilson 2007; Ripley 2009; Braga Goncalves et al. 2015a,b). Given these observations, it has been proposed that parental care in fishes may have evolved, at least partially, to protect developing embryos from hypoxia (Kolm and Ahnesjö 2005), possibly as a consequence of selection of larger egg sizes.…”

“…2007; Stölting and Wilson 2007; Ripley 2009; Ripley and Foran 2009; Braga Goncalves et al. 2015a) and preliminary evidence suggests that species with more complex brood pouches have larger eggs (Braga Goncalves et al. 2011).…”

Within species support for the expensive tissue hypothesis: a negative association between brain size and visceral fat storage in females of the Pacific seaweed pipefish

“…Previous studies of Syngnathidae and their reproductive biology have indicated that the physiological costs of male pregnancy become more evident in the later stage of the pregnancy (Goncalves et al. 2015; Paczolt and Jones 2015). Therefore, the lack of support for any costs of paternal care in light of investment into metabolically expensive organs should be taken with caution.…”

“…During this period, brooding males reduce food intake (Svensson 1988; Ahnesjo 1992) while they oxygenate (Goncalves et al. 2015), provide nutrition (Sagebakken et al. 2010; Kvarnemo et al.…”