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    Genetic population structures of common scavenging species near hydrothermal vents in the Okinawa Trough

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    Quantifying the feeding behavior and trophic impact of a widespread oceanic ctenophore

    This study provides quantitative data for Ocyropsis spp. feeding mechanisms and in situ data for gut contents during both day and night to begin assessing their trophic role in oceanic waters. Previous studies qualitatively described the feeding pattern of Ocyropsis spp.15 whereby this animal uses a unique capture mechanism among lobate ctenophores: direct transfer from lobe to mouth and encounters involving the mouth actively grabbing copepod prey24. These previous observations are confirmed as Ocyropsis spp. is able to deploy its dexterous, prehensile mouth to effectively capture prey within the lobes (Figs. 2, 3) and quantitative assessments of predation are also provided. It should be noted that while Ocyropsis spp. are known to occasionally consume a wide variety of prey types and sizes15, this study focuses only on copepod prey because our field data showed recognizable prey in Ocyropsis spp. guts was almost exclusively copepods.For example, mean speed of the mouth is less than 6 mm s−1 during predation events on copepods. Thus, while it may look rapid to the human eye, this is far below the escape swimming speeds exhibited by many copepods which are capable of moving at speeds of up to 500 mm s−125,26. Our observations show that the mechanism of capture is thus not reliant on grabbing copepods from the water between the ctenophore lobes with the mouth, but rather aided by copepod contact with the ctenophore lobes. Copepods between the lobes swam only with a speed of 7.94 mm s−1 (S.D. 7.25), to which the average mouth speed (5.83 mm s−1 (S.D. 1.68)) is comparable (Table 1). This suggests that Ocyropsis is able to reduce copepod swimming activity either by trapping them against the lobes (lobes respond to contact by prey) and/or the use of some form of adhesion or chemical that acts to reduce copepod activity. This unusual form of predation using a prehensile mouth allows Ocyropsis to be highly effective predators without the use of prey capturing tentillae seen in other lobate species.The presence of multiple prey has the potential to disrupt a raptorial type feeder such as Ocyropsis spp. more so than other lobates, since they lack tentillae, which would allow them to capture multiple prey simultaneously. Instead Ocyropsis spp. transfer one prey at a time directly from lobe to mouth15,27. So how is this ctenophore able to maintain such a high overall capture rate? The answer appears to be that Ocyropsis will modulate the number of attempts with the prehensile mouth depending on the number of prey present. For example, we did not observe any captures on the first attempt with the mouth with multiple prey, but the animals made up to 8 attempts at capturing the nearest copepod. This is in contrast to single copepod encounters in which ctenophores captured copepods on the first attempt 61% of the time and rarely made over 2 attempts, never exceeding 3 attempts (Figs. 3a, 5a, Table 1). This demonstrates Ocyropsis spp. can adjust its behavior to maintain high overall capture success when presented with multiple simultaneous prey. It is also interesting to note that the resulting increase in handling time due to making more attempts during multiple prey encounters is still lower than the handling time for most other lobates dealing with single prey27,28. It is not clear how often Ocyropsis spp. need to deal with multiple copepods simultaneously in nature, as oceanic waters contain characteristically low ctenophore prey densities compared to coastal zones9,29, however prey can be highly patchy and it appears that the unique prey capture mechanism of Ocyropsis spp. is still able to operate effectively in high density patches by increasing the number of attempts before aborting the attack which could serve as a means to maintain similar ingestion rates to single prey encounters.Typically, the feeding sequence of a ctenophore involves capture of prey in sticky colloblast cells and retraction of tentillae and/or ciliary transport of prey to the mouth15,27,30. These feeding mechanisms result in a range of handling times ranging from 2.5 s for Bolinopsis. infundibulum28 to nearly 22 min for Pleurobrachia bachei27. Capture rates can also be quite high, with overall capture success rates up to 74% for Mnemiopsis leidyi2,3. We found Ocyropsis has a relatively fast mean handling time of 6.3 s when a single copepod was present between the lobes, but handling time increased by approximately 2.5-fold if multiple prey were present. Overall capture success rates were comparable to the highly effective coastal ctenophore, M. leidyi, with a 71% success rate with single prey present and 81% capture rates if multiple prey were present between the lobes. Thus, Ocyropsis spp. are able to capture prey with high efficiency despite the differences in feeding mechanics compared to coastal lobate ctenophores. Additionally, since encounter rates of planktivores are directly related to the time spent searching for prey and time spent handling prey27, the relatively short handling time of Ocyropsis spp. and their direct feeding mechanism may allow them to sample more water and encounter a larger proportion of the available prey population than other species.Diel patterns of prey consumptionMany planktivorous species exhibit higher gut fullness at night31,32, due to higher prey availability in surface waters as a result of a diel vertical migration33,34. In situ gut content images showed that Ocyropsis spp. had a significantly higher gut fullness at night (12.4%) compared to during the day (4.2%) (Fig. 7). Ocyropsis spp. also had higher numbers of prey per individual gut at night, although overall biomass was not significantly different between night and day (Fig. 7). This can be explained by differences in prey characteristics; prey observed in the gut during the day were significantly larger (Table 2). This may be due to an ability to feed more selectively during the day since overall prey densities are lower. It should also be considered that turbulence in surface waters is, on average, much lower at night compared to daytime35 and that even small amounts of turbulence can negatively impact ctenophore feeding36,37. Therefore, smaller prey may have a higher likelihood of evading detection of Ocyropsis during the day compared to night, especially since these animals are most frequently observed in the upper 15 m of oceanic waters.Kremer, et al.38 estimates that O. crystallina requires 252 prey items to sustain itself. On average, Ocyropsis spp. in this study consume over 500 prey d−1. This exceeds their metabolic demands and suggests the observed population, on the western edge of the Gulf Stream, are likely to be actively growing and reproducing. The time required to digest prey items averaged 44 min for Ocyropsis which is faster than many, but not all, gelatinous zooplankton39,40,41. Digestion times of other gelatinous taxa span a range of times from 15 min to over 7 h at 20 °C40 and are impacted by size and number of prey per gut as well as temperature39,42,43. Digestion observations were performed at an ambient temperature of 25 °C and thus, these numbers represent a conservative estimate because the temperature of the water from which the animals were collected was 26.7–27.4 °C. Ocyropsis spp. would likely experience an increase in digestion rate with increased temperature.Digestion time was not impacted by the number of prey in the gut or by ctenophore body length. This differs from trends seen in other gelatinous taxa, such as A. aurita, M. leidyi, and B. infundibulum, where increasing body size resulted in faster digestion time39,40 and where increasing number of prey in the gut leads to longer digestion times39,40,41. In this study however, ctenophores were offered only a few copepods to ingest, thus it is likely they were not fed enough prey to satiate and slow the digestion process. Also worth considering is that the metabolic rate of O. crystallina does not appear to be affected by body size38. Though metabolic rates were not measured, this aligns with our finding that body size had no significant effect on digestion time. Analysis of in situ gut contents showed a significant positive logarithmic relationship between ctenophore length and total prey biomass per gut (Fig. 8). Individuals smaller than 20 mm in this study typically had fewer than the average number of copepods per gut (19), and larger individuals were the main driver of this relationship. This suggests that small Ocyropsis ( More

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    Familiarity, age, weaning and health status impact social proximity networks in dairy calves

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