Emersion in the mangrove forest fishRivulus marmoratus: a unique response to hydrogen sulfide

Few teleost fishes incubate embryos out of water, but the oxygen-rich terrestrial environment could provide advantages for early growth and development. We tested the hypothesis that embryonic oxygen uptake is limited in aquatic environments relative to air using the selffertilizing amphibious mangrove rivulus, Kryptolebias marmoratus, which typically inhabits hypoxic, water-filled crab burrows. We found that adult mangrove rivulus released twice as many embryos in terrestrial versus aquatic environments and that air-reared embryos had accelerated developmental rates. Surprisingly, air-reared embryos consumed 44% less oxygen and possessed larger yolk reserves, but attained the same mass, length and chorion thickness. Water-reared embryos moved their opercula ∼2.5 more times per minute compared with air-reared embryos at 7 days post-release, which probably contributed to the higher rates of oxygen uptake and yolk utilization we observed. Genetically identical air-and waterreared embryos from the same parent were raised to maturity, but the embryonic environment did not affect growth, reproduction or emersion ability in adults. Therefore, although aspects of early development were plastic, these early differences were not sustained into adulthood. Kryptolebias marmoratus embryos hatched out of water when exposed to aerial hypoxia. We conclude that exposure to a terrestrial environment reduces the energetic costs of development partly by reducing the necessity of embryonic movements to dispel stagnant boundary layers. Terrestrial incubation of young would be especially beneficial to amphibious fishes that occupy aquatic habitats of poor water quality, assuming low terrestrial predation and desiccation risks.

Section: Discussionsupporting

confidence: 90%

Fish embryos on land: terrestrial embryo deposition lowers oxygen uptake without altering growth or survival in the amphibious fishKryptolebias marmoratus

Wells

Turko

Wright

2015

“…The mangrove rivulus, Kryptolebias marmoratus Poey 1880 (Cyprinodontiformes), is an amphibious fish that makes temporary excursions onto land for various reasons: actively pursuing prey at the water-land interface, purposefully leaving the water as a result of poor conditions such as high levels of hydrogen sulfide or anoxia, being stranded at low tide or escaping an aquatic predator (Abel et al, 1987;Regan et al, 2011;Pronko et al, 2013). Minnows, gobies, sculpins and some other groups of teleost fishes are also capable of finding themselves on land through active and passive means (Gibb et al, 2013).…”

Section: Introductionmentioning

confidence: 99%

By land or by sea: a modified C-start motor pattern drives the terrestrial tail-flip

Perlman

Ashley‐Ross

2016

Aquatic C-start escape responses in teleost fishes are driven by a wellstudied network of reticulospinal neurons that produce a motor pattern of simultaneous contraction of axial muscle on the side of the body opposite the threatening stimulus, bending the fish into the characteristic C shape, followed by a traveling wave of muscle contraction on the contralateral side that moves the fish away from the threat. Superficially, the kinematics of the terrestrial tail-flip resemble the C-start, with the anterior body rolling up and over the tail into a tight C shape, followed by straightening as the fish launches off of the caudal peduncle into ballistic flight. We asked whether similar motor control is used for both behaviors in the amphibious mangrove rivulus, Kryptolebias marmoratus. Fine-wire bipolar electrodes were percutaneously inserted into repeatable paired axial locations in five individual fish. Electromyograms synchronized with high-speed video were made of aquatic C-starts, immediately followed by terrestrial tail-flips. Tail-flips took longer to complete than aquatic escapes; correspondingly, muscles were activated for longer durations on land. In the tail-flip, activity was seen in contralateral posterior axial muscle for an extended period of time during the formation of the C shape, likely to press the caudal peduncle against the ground in preparation for launch. Tail-flips thus appear to be produced by modification of the motor pattern driving the aquatic C-start, with differences consistent with the additional requirement of overcoming gravity.

“…The mangrove rivulus Kryptolebias marmoratus [formerly Rivulus marmoratus (Poey 1880)] is an amphibious fish native to mangrove swamps ranging from central Florida to northern Brazil (Davis et al, 1990). These small, fusiform teleosts of the order Cyprinodontiformes are notable for their ability to fully emerse from the water when conditions are poor (Abel et al, 1987;Taylor, 2000). Tidal fluctuations, elevated hydrogen sulfide levels and anoxic water conditions are common in upland mangrove environments (Harrington, 1961).…”

Section: Introductionmentioning

confidence: 99%

“…Tidal fluctuations, elevated hydrogen sulfide levels and anoxic water conditions are common in upland mangrove environments (Harrington, 1961). Mangrove rivulus respond to high sulfide levels and low oxygen levels with a threshold-mediated emersion behavior (Abel et al, 1987;Regan et al, 2011). Taylor (Taylor, 2000) has also tied emersion events to intraspecific competition.…”

Section: Introductionmentioning

confidence: 99%

“…Kryptolebias marmoratus have the ability to respire cutaneously, a trait well suited for their habitat and emersion behaviors (Grizzle and Thiyagarajah, 1987). Abel et al (Abel et al, 1987) showed that K. marmoratus can survive out of the water for more than 30days in moist leaf litter, and Taylor (Taylor, 1990) witnessed terrestrial survivability of 66days in an artificial muddy environment. Kryptolebias marmoratus have recently been found concentrated inside of logs far removed from the water, with anywhere from a dozen to 100 individuals in a single log (Taylor et al, 2008).…”

Section: Introductionmentioning

confidence: 99%

See 1 more Smart Citation

Launches, squiggles and pounces, oh my! The water–land transition in mangrove rivulus (Kryptolebias marmoratus)

Pronko

Perlman

Ashley‐Ross

2013

SUMMARYMangrove rivulus (Kryptolebias marmoratus) are small fusiform teleosts (Cyprinodontiformes) with the ability to locomote on land, despite lacking apparent morphological adaptations for terrestrial movement. Rivulus will leave their aquatic habitat for moist, terrestrial environments when water conditions are poor, or, as we show here, to capture terrestrial insects. Specimens were conditioned to eat pinhead crickets on one side of their aquaria. After 2weeks of conditioning, a barrier with a slope of 15deg was partially submerged in the middle of the tank, forcing the fish to transition from water to land and back into water in order to feed. Kinematics during the transition were recorded using Fastec high-speed video cameras (125-250framess -1 ). Videos were analyzed using Didge and ImageJ software programs. Transition behaviors were characterized and analyzed according to their specific type. Body oscillation amplitude and wave duration were quantified for movements along the substrate, along with initial velocity for launching behaviors. Kryptolebias marmoratus used a diverse suite of behaviors to transition from water to land. These behaviors can be categorized as launches, squiggles and pounces. Prey were captured terrestrially and brought underwater for consumption. Kryptolebias marmoratus's suite of behaviors represents a novel solution to non-tetrapodal terrestrial transition, which suggests that fishes may have been able to exploit land habitats transiently, without leaving any apparent evidence in the fossil record. Supplementary material available online at