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

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.