Evidence of paternal nutrient provisioning to embryos in broad‐nosed pipefish <i>Syngnathus typhle</i>

Kvarnemo, Charlotta; Mobley, Kenyon B.; Partridge, Charlyn; Jones, Adam G.; Ahnesjö, Ingrid

doi:10.1111/j.1095-8649.2011.02989.x

Cited by 58 publications

(54 citation statements)

References 39 publications

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“…These results highlight a potential O 2 limitation to brooding within the closed environment of the brood pouch. The evolution of the brood pouch among syngnathids has been conceptually linked to more advanced types of care because of the potential to osmoregulate (Quast and Howe, 1980;Carcupino et al, 1997Carcupino et al, , 2002Partridge et al, 2007;Ripley, 2009) and to provide nutrients (Haresign and Shumway, 1981;Ripley andForan, 2006, 2009;Kvarnemo et al, 2011) to the developing youngabilities that are limited in species that do not have brood pouches (Berglund et al, 1986b;Carcupino et al, 2002). Therefore, it is important to note that, in terms of oxygenation, the presence of a brood pouch is here shown to limit, not ease, embryo access to O 2 and thus limit their development.…”

Section: Discussionmentioning

confidence: 99%

“…More complex brood pouches enable males to physically protect the embryos from external factors such as predators, and to provision them with nutrients, osmoregulation and oxygenation during brooding (Wilson et al, 2001). Male provisioning of nutrients to the developing young has been shown in a number of pipefish species (Haresign and Shumway, 1981;Ripley andForan, 2006, 2009;Kvarnemo et al, 2011). Also, the function of the brood pouch in osmoregulation is well established (Quast and Howe, 1980;Carcupino et al, 1997;Partridge et al, 2007;Ripley, 2009).…”

Section: Introductionmentioning

confidence: 99%

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Embryo oxygenation in pipefish brood pouches: novel insights

Gonçalves

Ahnesjö

Kvarnemo

2015

Journal of Experimental Biology

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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.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Embryo oxygenation in pipefish brood pouches: novel insights

Gonçalves

Ahnesjö

Kvarnemo

2015

Journal of Experimental Biology

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“…1986b; Ripley and Foran 2006; Ripley 2009; Kvarnemo et al. 2011). Furthermore, species with enclosed brood pouches (e.g., Syngnathus spp.…”

Section: Introductionmentioning

confidence: 99%

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

Gonçalves

Ahnesjö

Kvarnemo

2016

Ecology and Evolution

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For animals that reproduce in water, many adaptations in life‐history traits such as egg size, parental care, and behaviors that relate to embryo oxygenation are still poorly understood. In pipefishes, seahorses and seadragons, males care for the embryos either in some sort of brood pouch, or attached ventrally to the skin on their belly or tail. Typically, egg size is larger in the brood pouch group and it has been suggested that oxygen supplied via the pouch buffers the developing embryos against hypoxia and as such is an adaptation that has facilitated the evolution of larger eggs. Here, using four pipefish species, we tested whether the presence or absence of brood pouch relates to how male behavior, embryo size, and survival are affected by hypoxia, with normoxia as control. Two of our studied species Entelurus aequoreus and Nerophis ophidion (both having small eggs) have simple ventral attachment of eggs onto the male trunk, and the other two, Syngnathus typhle (large eggs) and S. rostellatus (small eggs), have fully enclosed brood pouches on the tail. Under hypoxia, all species showed lower embryo survival, while species with brood pouches suffered greater embryo mortality compared to pouchless species, irrespective of oxygen treatment. Behaviorally, species without pouches spent more time closer to the surface, possibly to improve oxygenation. Overall, we found no significant benefits of brood pouches in terms of embryo survival and size under hypoxia. Instead, our results suggest negative effects of large egg size, despite the protection of brood pouches.

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“…Together with the fact that it provides extensive parental care and lives in an environment with naturally high variability in O 2 levels [38 -41], these characteristics make it a very apt model organism. As is typical for many pipefishes and seahorses (Syngnathidae), males of this genus care for the developing embryos in a sealed brood pouch where they protect, osmoregulate, oxygenate and transfer nutrients to the embryos through the vascularized walls of the pouch [37,[42][43][44][45]. Moreover, previous work on S. typhle has shown that larger embryos have higher respiration rates than smaller ones [46], larger eggs result in larger offspring [47] and that larger juveniles enjoy fitness benefits [48].…”

Section: Introductionmentioning

confidence: 99%

The evolutionary puzzle of egg size, oxygenation and parental care in aquatic environments

2015

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Offspring fitness generally improves with increasing egg size. Yet, eggs of most aquatic organisms are small. A common but largely untested assumption is that larger embryos require more oxygen than they can acquire through diffusion via the egg surface, constraining egg size evolution. However, we found no detrimental effects of large egg size on embryo growth and survival under hypoxic conditions. We tested this in the broad-nosed pipefish, Syngnathus typhle, whose males provide extensive care (nourishment, osmoregulation and oxygenation) to their young in a brood pouch on their bodies. We took advantage of this species' pronounced variation in egg size, correlating positively with female size, and tested the effect of hypoxia (40% dissolved oxygen) versus fully oxygenated (100%) water on embryo size and survival of large versus small eggs after 18 days of paternal brooding. Egg size did not affect embryo survival, regardless of O 2 treatment. While hypoxia affected embryo size negatively, both large and small eggs showed similar reductions in growth. Males in hypoxia ventilated more and males with large eggs swam more, but neither treatment affected their position in the water column. Overall, our results call into question the most common explanation for constrained egg size evolution in aquatic environments.

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Evidence of paternal nutrient provisioning to embryos in broad‐nosed pipefish Syngnathus typhle

Cited by 58 publications

References 39 publications

Embryo oxygenation in pipefish brood pouches: novel insights

Embryo oxygenation in pipefish brood pouches: novel insights

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

The evolutionary puzzle of egg size, oxygenation and parental care in aquatic environments

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