Embryonic motility and hatching success of Ambystoma maculatum are influenced by a symbiotic alga

Abstract

To augment O2 supply through the jelly mass and egg capsule, embryonic yellow-spotted salamanders ( Ambystoma maculatum (Shaw, 1802)) take advantage of a unicellular alga, Oophila ambystomatis . Convective currents from surface cilia, however, may also enhance O2 transport, whereas muscular contractions could either enhance delivery or contribute to O2 consumption. Embryonic motion is, therefore, potentially vital to salamander development. We examined embryonic motility across multiple developmental stages, survivorship, and hatching timing in response to different algal levels by rearing salamander egg masses under three different diel light cycles: 24 h dark, 12 h light, and 24 h light per day. Embryos raised in continuous light hatched synchronously and at slightly earlier developmental stages than embryos raised in the dark or in 12 h light per day. We removed eggs at multiple stages to examine embryonic rotation and muscular contraction rates under 180 min periods of both light and dark. Rotational movements occurred more frequently in alga-free than in algae-inhabited eggs, and more frequently in algae-inhabited eggs in the dark than in light. At later developmental stages, muscular contractions were more frequent in embryos from algae-inhabited egg masses in light than those in the dark; thus embryos with less O2 reduced muscular activity, thereby reducing energy consumption when O2 availability was compromised.

Intracellular invasion of green algae in a salamander host

“…The mutual benefit of this facultative association has been clearly established through exclusion experiments. Clutches raised in the dark do not accrue detectable algae (6)(7)(8)(9). The presence of algae in these experiments correlates with earlier hatching (6, 9), decreased embryonic mortality (7,8), more synchronous hatching (8,9), and reaching a larger size (8) and later developmental stage (9) at hatching.…”

“…Clutches raised in the dark do not accrue detectable algae (6)(7)(8)(9). The presence of algae in these experiments correlates with earlier hatching (6, 9), decreased embryonic mortality (7,8), more synchronous hatching (8,9), and reaching a larger size (8) and later developmental stage (9) at hatching. Additionally, algal growth is minimal in egg capsules after embryos are removed (8), indicating that the embryos, and not the egg capsules, aid algal growth.…”

“…These observations suggest that intracapsular algal cells in our samples comprise a single species. The published literature on this association (6,8,9) refers to the algae as "Oophila amblystomatis" (Lambert ex Printz) (19) on the basis of an informal species designation by Lambert (6), although-to date-no formal taxonomic description exists. Previous studies reported additional bacteria and protists within the egg capsules (6,14).…”

“…The reciprocal benefits of hatchling survival and growth to the embryo, and population growth to the algae, reveal that this symbiosis is a true mutualism (6,8,9). However, the material benefit of algal symbionts has been controversial.…”

“…11-13; however, others (14) found no oxygen benefit using older techniques]. Presence of the algae also correlates with decreased cilium-mediated rotation of early-stage embryos and increased muscular contractions during later embryonic stages (9), both of which may be secondary effects of modulated oxygen levels.…”