Pre-hatching development in the intertidal zone negatively affects juvenile survival and physiology in the muricid gastropod Acanthina monodon

Chaparro, Óscar R.; Salas-Yanquin, L.P.; Matos, Alisson Sousa; Büchner-Miranda, J.A.; Gray, Matthew W.; Cubillos, V.; Pechenik, Jan A.

doi:10.1007/s00227-018-3412-1

Cited by 11 publications

(6 citation statements)

References 35 publications

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“…Intertidal egg capsules are exposed to lower and higher temperatures, UV irradiation, water loss, changes in salinity, pH and oxygen concentrations, than subtidal capsules (Chaparro et al 2018). Therefore, encapsulated embryos that develop in the intertidal zone are subjected to greater levels of stress than those developing in the subtidal zone.…”

Section: Discussionmentioning

confidence: 99%

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Reproductive pattern of Trochita pileolus (d' Orbigny, 1841) (Gastropoda: Calyptraeidae) and different types of intracapsular development in Trochita species of South America

et al. 2021

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Several types of development are reported in the worldwide distributed Family Calyptraeidae. In species with direct development, embryos can grow from large eggs or can feed on nurse eggs, nurse embryos, or other intracapsular nutritional resources. Here the reproductive mode of Trochita pileolus and how biochemical composition varies among egg size between three species of Trochita were studied. Adults and broods of T. pileolus were collected off Tierra del Fuego and nearby Burdwood Bank at depths of 96-151 m. The mean shell diameter of brooding females was 16.3 ± 2 mm and the number of egg capsules observed ranged from 5 to 9. In each egg capsule 7-10 embryos developed from uncleaved eggs of about 500 µm diameter. Neither nurse eggs nor other kinds of extraviteline food sources were recorded. No oophagy, adelphophagy, or late intracapsular cannibalism were observed. The development mode of T. pileolus closely resembles that of the giant T. trochiformis from Chile, in which the energy for developing embryos is obtained from large fertile eggs. The eggs of T. trochiformis had higher lipid content than the other two species and were more energy-dense than glycogen-enriched eggs. The relative lipid coverage area and the hatching size of T. pileus were similar to T. pileolus, although the egg size was three times smaller. This could be attained because T. pileus has developed intracapsular nutritional resources such as nurse eggs and adelphophagy.

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Section: Discussionmentioning

confidence: 99%

“…This evolutionary pathway may have developed because of a difference in the habitat of these species. Trochita trochiformis inhabits the intertidal zone, where the embryonic mortality is higher (Chaparro et al 2018); so this species lays more egg capsules with more eggs in each reproductive event and in consequence the fecundity increases.…”

Section: Discussionmentioning

confidence: 99%

Reproductive pattern of Trochita pileolus (d' Orbigny, 1841) (Gastropoda: Calyptraeidae) and different types of intracapsular development in Trochita species of South America

et al. 2021

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“…If simultaneously exposed to cadmium (Cd), however, embryos took longer to develop and experienced higher mortality rates. Early development is often the most vulnerable life stage to stressors, and sublethal effects during development can manifest in later life stages (Chaparro et al, 2018;Pineda et al, 2012;Salas-Yanquin et al, 2022).…”

Section: Discussionmentioning

confidence: 99%

“…These stressors also increase the toxicity of heavy metal pollutants resulting in abnormal development (Boukadida et al, 2016;Gamain et al, 2016;Kimberly & Salice, 2014a). Sub-lethal effects during these young life stages can permanently reduce the fitness of the organism (Chaparro et al, 2018;Rouchon & Phillips, 2017b). The consequences of sublethal exposure are often more extreme in early life stages, as reductions in growth rate increase the risk of subsequent mortality and reduce dispersal potential (Marshall & Keough, 2007.…”

Section: Effects Of Pollution On Reproduction and Early Life Stagesmentioning

confidence: 99%

“…Early developmental stages of organisms are often the most sensitive to stressors (Gomot, 1998;Pineda et al, 2012;Kimberly & Salice, 2013). Stress can result in increased mortality, developmental abnormalities, and decreased rates of development (Chaparro et al, 2018;Gallardo & Cancino, 2009;Przeslawski et al, 2015). In species with planktonic development, these early stages occur in direct contact with water-borne pollutants.…”

Section: Introductionmentioning

confidence: 99%

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Heavy metals and reproduction in the benthic carnivore, Cominella glandiformis.

Duncan¹

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Heavy metal pollution is a growing concern for aquatic ecosystems world-wide. Heavy metals are introduced to waterways via direct run off from land, storm drains and (for coastal environments) river and stream outflows. Offspring of species with benthic development have low dispersal potential, so are likely to experience the same conditions as their parents. Little is known about the effects of heavy metal pollution on these embryos in a marine context. I use the mud whelk Cominella glandiformis to examine the effects of the common heavy metals copper (Cu) and zinc (Zn) on aspects of foraging ability, condition and reproduction in adults, and growth and survival in encapsulated embryos and recently hatched juveniles. This species has an entirely benthic lifecycle, and occurs in a habitat prone to pollution, making it an ideal model species with which to examine the effects of ongoing heavy metal pollution. In Chapter 2, I describe the reproductive patterns of Cominella glandiformis collected from two local sites and kept in the laboratory. Females from both sites laid a similar number of capsules and showed similar maternal investment. The average capsule was 1.06 mm3 and contained 5 eggs of 0.28 mm diameter. Larger females had a higher fecundity than smaller females, producing larger capsules containing larger eggs. Previous research on C. glandiformis has relied on field-collected capsules, which could not be attributed to females. This chapter complements previous research on related rocky shore species (C. maculosa and C. virgata), finding consistent maternal investment across females. Further, this refines the existing understanding of reproduction in this species. In Chapter 3, I examine the effects of pollutant mixture (Cu-only or Cu+Zn; 50 µg Cu L-1 and 100 µg Zn L-1) and pathway (aqueous-only or aqueous+dietary) on aspects of adult whelk physiology and foraging ability. I exposed whelks to the above treatments for four weeks, measuring their respiration, food consumption and weight loss throughout. Pollutant pathway did not affect physiological stress, but pollutant mixture did. Copper polluted whelks reduced their food intake yet gained weight, suggesting that they prioritised present growth over future energy stores. After the four-week exposure, I tested the effects of metal exposure on foraging ability and preferences in a subset of whelks. Polluted whelks preferred contaminated prey, showed impaired foraging efficiency. The pollution pathway had little effect on response variables in this study, though the addition of Zn may have reduced the growth-response seen in Cu-exposed whelks. Overall, these results indicate that pollution may leave whelks in poor condition prior to the breeding season, impairing their reproductive fitness. In Chapter 4, I use C. glandiformis as a model species to examine the effects of heavy metals on the reproduction of a benthic carnivore with a benthic lifecycle. I exposed adult C. glandiformis to one of five heavy metal treatments (plus control) and examined their subsequent rates of capsule laying and indicators of maternal investment. Some continued development in the same pollution conditions as the female, allowing comparisons of survival, development time, and hatching size. Whelks exposed to >5 µg Cu L-1 began laying three weeks later than Control whelks, though a similar number of capsules were laid overall. Whelks showed similar maternal investment, laying similarly sized capsules containing approximately six eggs which developed in to six hatchlings. Eggs and hatchlings were similar sizes, though ≤3.5% of capsules hatched from the two most extreme treatments. The development time of capsules (i.e. time from laying to hatching) decreased through the season. Later laying by polluted whelks was associated with faster development, possibly due to warmer water temperatures. Consistent with previous Cominella research using starved females, these results suggest that females invest similarly in capsules, irrespective of adult stress experience. In Chapter 5, I examine the effects of heavy metals on the development and post-hatching growth and survival of C. glandiformis. All embryos exposed to 50 µg Cu L-1 died at early multicellular stages within the first three weeks. Those exposed to 20 µg Cu L-1 (with or without 50 µg Zn L-1) showed reduced growth rates compared to Controls and died before reaching the veliger stage. Juvenile whelks were unaffected by pollution, with similar survival and growth to Control juveniles after 5 weeks. This chapter agrees with previous findings that embryos are more sensitive than juveniles and suggests that recently hatched juveniles may be similarly tolerant of metals as adults. My thesis uses laboratory-based experiments to assess the response of a benthic predator from a pollution-prone ecosystem to realistic heavy metal concentrations. Overall, C. glandiformis is highly tolerant of Zn. Pollution impaired adult condition and foraging ability, which likely reduces reproductive output. My results suggest that mothers do not pre-empt the conditions that their offspring will experience, resulting in reduced embryonic growth and survival. Pollution-naïve juveniles may be similarly tolerant of moderate Cu and Zn as adults. Thus, as demonstrated in other species, the early, encapsulated stages are the most vulnerable life stage to pollution. Overall, my thesis represents one of few detailed examinations of reproduction in a marine benthic developer exposed to pollution. Further, it advances our understanding of the reproduction of this common, endemic intertidal predator.

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Latent effects of intertidal encapsulated development on juvenile fitness of the marine snail Acanthina monodon

et al. 2022

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Pre-hatching development in the intertidal zone negatively affects juvenile survival and physiology in the muricid gastropod Acanthina monodon

Cited by 11 publications

References 35 publications

Reproductive pattern of Trochita pileolus (d' Orbigny, 1841) (Gastropoda: Calyptraeidae) and different types of intracapsular development in Trochita species of South America

Reproductive pattern of Trochita pileolus (d' Orbigny, 1841) (Gastropoda: Calyptraeidae) and different types of intracapsular development in Trochita species of South America

Heavy metals and reproduction in the benthic carnivore, Cominella glandiformis.

Latent effects of intertidal encapsulated development on juvenile fitness of the marine snail Acanthina monodon

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