ABSTRACT We describe, for the first time, egg masses and larval developmental mode of a recently described Antarctic philinoid snail, Waegelea antarctica. Egg masses resembled the gelatinous, attached masses of many temperate philinoid species and contained very large offspring that hatched as developmentally advanced veligers with many juvenile features. Like other Antarctic heterobranch egg masses, development in the masses of W. antarctica appeared to be largely synchronous despite low internal oxygen levels. Hatched larvae could both swim and crawl, and we did not observe metamorphosis over several days. Molecular barcoding using cytochrome c oxidase subunit I (COI) showed an almost perfect (<0.002% difference) match between our specimens from McMurdo Sound in the Ross Sea and a single sequence from a specimen collected >8,000 km away in the Weddell Sea, suggesting either high realized larval dispersal or a recent range expansion. We also describe the egg mass of the related Antarctophiline alata (identified using COI barcoding) from the Ross Sea, which differed from published descriptions in having considerably smaller embryos.
more »
« less
Extraordinarily long development of the Antarctic gastropod Antarctodomus thielei (Neogastropoda: Buccinoidea)
Antarctic animals share many traits that are attributed to evolution in a stable, extremely cold climate. Among invertebrates, development is exceptionally slow, making observational studies of development logistically challenging, particularly when conducted under natural conditions in the field. Using multiple deployments to McMurdo Station, Antarctica, we characterized the development, in the field, of an unidentified buccinoidean gastropod species with encapsulated development. Thirteen egg capsules collected at Granite Harbor, McMurdo Sound, Ross Sea, were attached to natural rock and outplanted at a depth of ~25 m at the base of the McMurdo Intake Jetty on 2 December 2007, photographed on 5 October 2011 and 6 September 2012 and then returned to the laboratory on 27 November 2015. In 2015, four capsules were open and empty, five were open and contained a single large hatchling and the remaining four capsules were intact but not open, each containing a single large juvenile snail. To identify the developing embryos, we sequenced mitochondrial cytochrome c oxidase subunit I (COI) from two hatchlings and compared those sequences with those from adults collected near the egg mass, as well as with sequences of other buccinoideans from GenBank. Based on the close match between hatchling and adult COI sequences (hatchling sequences differed from those of an adult at only 2 of 658 nucleotide positions), we identified the embryos as Antarctodomus thielei (Powell, 1958)). The egg mass morphology and development of this species have not been previously described. Our study shows that A. thielei has a development time of more than 8 years, which is the longest measured for any gastropod.
more » « less- NSF-PAR ID:
- 10117638
- Publisher / Repository:
- Oxford University Press
- Date Published:
- Journal Name:
- Journal of Molluscan Studies
- Volume:
- 85
- Issue:
- 3
- ISSN:
- 0260-1230
- Page Range / eLocation ID:
- p. 319-326
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
more » « less
Abstract Vertebrate embryos require access to water; however, many species nest in terrestrial habitats that vary considerably in moisture content. Oviparous, non‐avian reptiles have served as models to understand how environmental factors, like moisture availability, influence development because eggs are often exposed to prevailing environments in the absence of parental care. Though much research demonstrates the importance of water absorption by eggs, many ecological factors that influence moisture availability in natural nests have received little attention. For example, the type of substrate in which nests are constructed is understudied. We experimentally incubated eggs of the brown anole lizard (
Anolis sagrei ) in 2 naturally occurring nest substrates that were treated with varying amounts of water to determine how natural substrates influence development at different moisture concentrations. One substrate consisted of sand and crushed seashells and the other was mostly organic material (i.e. decayed plant material). Both are common nesting substrates at our field site. When controlling for water uptake by eggs, we found that egg survival and hatchling phenotypes were similar between substrates; however, embryos developed more quickly in the sand/shell substrate than the organic substrate, indicating substrate‐specific effects on embryo physiology. These results demonstrate that different natural substrates can result in similar developmental outcomes if the water available to eggs is comparable; however, some aspects of development, like developmental rate, are affected by the type of substrate, independent of water availability. Further study is required to determine how natural substrates influence embryo physiology independent of water content. -
The phenology of critical biological events in aquatic ecosystems are rapidly shifting due to climate change. Growing variability in phenological cues can increase the likelihood of trophic mismatches, causing recruitment failures in commercially, culturally, and recreationally important fisheries. We tested for changes in spawning phenology of regionally important walleye (Sander vitreus) populations in 194 Midwest US lakes in Minnesota, Michigan, and Wisconsin spanning 1939-2019 to investigate factors influencing walleye phenological responses to climate change and associated climate variability, including ice-off timing, lake physical characteristics, and population stocking history. Data from Wisconsin and Michigan lakes (185 and 5 out of 194 total lakes, respectively) were collected by the Wisconsin Department of Natural Resources (WDNR) and the Great Lakes Indian Fish and Wildlife Commission (GLIFWC) through standardized spring walleye mark-recapture surveys and spring tribal harvest season records. Standardized spring mark-recapture population estimates are performed shortly after ice-off, where following a marking event, a subsequent recapture sampling event is conducted using nighttime electrofishing (typically AC – WDNR, pulsed-DC – GLIFWC) of the entire shoreline including islands for small lakes and index stations for large lakes (Hansen et al. 2015) that is timed to coincide with peak walleye spawning activity (G. Hatzenbeler, WDNR, personal communication; M. Luehring, GLIFWC, personal communication; Beard et al. 1997). Data for four additional Minnesota lakes were collected by the Minnesota Department of Natural Resources (MNDNR) beginning in 1939 during annual collections of walleye eggs and broodstock (Schneider et al. 2010), where date of peak egg take was used to index peak spawning activity. For lakes where spawning location did not match the lake for which the ice-off data was collected, the spawning location either flowed into (Pike River) or was within 50 km of a lake where ice-off data were available (Pine River) and these ice-off data were used. Following the affirmation of off-reservation Ojibwe tribal fishing rights in the Ceded Territories of Wisconsin and the Upper Peninsula of Michigan in 1987, tribal spearfishers have targeted walleye during spring spawning (Mrnak et al. 2018). Nightly harvests are recorded as part of a compulsory creel survey (US Department of the Interior 1991). Using these records, we calculated the date of peak spawning activity in a given lake-year as the day of maximum tribal harvest. Although we were unable to account for varying effort in these data, a preliminary analysis comparing spawning dates estimated using tribal harvest to those determined from standardized agency surveys in the same lake and year showed that they were highly correlated (Pearson’s correlation: r = 0.91, P < 0.001). For lakes that had walleye spawning data from both agency surveys and tribal harvest, we used the data source with the greatest number of observation years. Ice-off phenology data was collected from two sources – either observed from the Global Lake and River Ice Phenology database (Benson et al. 2000)t, or modeled from a USGS region-wide machine-learning model which used North American Land Data Assimilation System (NLDAS) meteorological inputs combined with lake characteristics (lake position, clarity, size, depth, hypsography, etc.) to predict daily water column temperatures from 1979 - 2022, from which ice-off dates could be derived (https://www.sciencebase.gov/catalog/item/6206d3c2d34ec05caca53071; see Corson-Dosch et al. 2023 for details). Modeled data for our study lakes (see (Read et al. 2021) for modeling details), which performed well in reflecting ice phenology when compared to observed data (i.e., highly significant correlation between observed and modeled ice-off dates when both were available; r = 0.71, p < 0.001). Lake surface area (ha), latitude, and maximum depth (m) were acquired from agency databases and lake reports. Lake class was based on a WDNR lakes classification system (Rypel et al. 2019) that categorized lakes based on temperature, water clarity, depth, and fish community. Walleye stocking history was defined using the walleye stocking classification system developed by the Wisconsin Technical Working Group (see also Sass et al. 2021), which categorized lakes based on relative contributions of naturally-produced and stocked fish to adult recruitment by relying heavily on historic records of age-0 and age-1 catch rates and stocking histories. Wisconsin lakes were divided into three groups: natural recruitment (NR), a combination of stocking and natural recruitment (C-ST), and stocked only (ST). Walleye natural recruitment was indexed as age-0 walleye CPE (number of age-0 walleye captured per km of shoreline electrofished) from WDNR and GLIFWC fall electrofishing surveys (see Hansen et al. 2015 for details). We excluded lake-years where stocking of age-0 fish occurred before age-0 surveys to only include measurements of naturally-reproduced fish.more » « less
-
more » « less
Abstract Phenotypic variation within populations is influenced by the environment via plasticity and natural selection. How phenotypes respond to the environment can vary among traits, populations and life stages in ways that can influence fitness.
Plastic responses during early development are particularly important because they can affect components of fitness throughout an individual's life. Consequently, how natural selection shapes developmental plasticity could be influenced by fitness consequences across different life stages. Moreover, spatial variation in selection pressures could generate differences in plastic responses among populations.
To gain insight into sources of variation in phenotypes and survival, we used a laboratory egg incubation experiment using brown anole lizards
Anolis sagrei from mainland (ancestral) and island (descendent) populations, combined with a mark–release–recapture experiment in the field. Our study was designed to (a) quantify the effects developmental temperature on embryo development and offspring morphology, (b) assess how developmental temperature influences offspring survival across different life stages and (c) quantify how thermal reaction norms vary among ancestral and descendant populations.Developmental temperature influenced offspring morphology, but thermal reaction norms of embryos showed little variation among populations. Developmental temperature influenced offspring survival, but the patterns differed between embryo and hatchling stages; the optimal temperature for embryos was about 5℃ lower than that for hatchlings. High temperatures were thermally stressful to embryos, but they reduced incubation duration and led to early hatching. In turn, earlier hatching increased the probability of survival to adulthood. Moreover, the effect of developmental temperature on hatchling survival was most pronounced for offspring that hatched late in the season.
The difference in optimal developmental temperatures between life stages may be driven by physiological tolerance for embryos and by ecological factors for hatchlings. Moreover, the fitness consequences of the developmental environment depend on the phenology of hatching. Overall, these results highlight how the developmental environment can differentially affect fitness across life stages and show that temporal thermal heterogeneity can influence survival of embryos, but the consequences on post‐hatching stages may vary at different times of the season.
A free
Plain Language Summary can be found within the Supporting Information of this article. -
more » « less
Abstract Migratory, long‐lived animals are an important focus for life‐history theory because they manifest extreme trade‐offs in life‐history traits: delayed maturity, low fecundity, variable recruitment rates, long generation times, and vital rates that respond to variation across environments. Galapagos tortoises are an iconic example: they are long‐lived, migrate seasonally, face multiple anthropogenic threats, and have cryptic early life‐history stages for which vital rates are unknown. From 2012 to 2021, we studied the reproductive ecology of two species of Galapagos tortoises (
Chelonoidis porteri andC. donfaustoi ) along elevation gradients that coincided with substantial changes in climate and vegetation productivity. Specifically, we (1) measured the body and reproductive condition of 166 adult females, (2) tracked the movements of 33 adult females using global positioning system telemetry, and monitored their body condition seasonally, (3) recorded nest temperatures, clutch characteristics, and egg survival from 107 nests, and (4) used radiotelemetry to monitor growth, survival, and movements of 104 hatchlings. We also monitored temperature and rainfall from field sites, and remotely sensed primary productivity along the elevation gradient. Our study showed that environmental variability, mediated by elevation, influenced vital rates of giant tortoises, specifically egg production by adult females and juvenile recruitment. Adult females were either elevational migrants or year‐round lowland residents. Migrants had higher body condition than residents, and body condition was positively correlated with the probability of being gravid. Nests occurred in the hottest, driest parts of the tortoise's range, between 6 and 165 m elevation. Clutch size increased with elevation, whereas egg survival decreased. Hatchling survival and growth were highest at intermediate elevations. Hatchlings dispersed rapidly to 100–750 m from their nests before becoming sedentary (ranging over <0.2 ha). Predicted future climates may impact the relationships between elevation and vital rates of Galapagos tortoises and other species living across elevation gradients. Resilience will be maximized by ensuring the connectivity of foraging and reproductive areas within the current and possible future elevational ranges of these species.
