Relating chronic toxicity responses to population-level effects: A comparison of population-level parameters for three salmon species as a function of low-level toxicity

Standard laboratory toxicity tests assess the physiological responses of individual organisms to exposure to toxic substances under controlled conditions. Time and space restrictions often prevent the assessment of population-level responses to a toxic substance. Contaminants can affect various biological functions (e.g. growth, fecundity or behavior), which may alter different demographic traits, leading to population-level impacts. In this study, immune suppression, reproductive dysfunction and somatic growth impairment were examined using life history matrix models for coho salmon (Oncorhynchus kisutch), sockeye salmon (Oncorhynchus nerka) and chinook salmon (Oncorhynchus tshawytscha). Our intent was to gauge the relative magnitude of response to toxic effects among species and between life history stages, not provide a specific estimate of population growth rate or abundance. Effects due to immune suppression were modeled as reductions in age-specific survival. Toxic impacts on reproductive function were modeled as a 10% reduction in reproductive contribution for all reproductively mature age groups. Model runs that examined the effect of somatic growth reduction on population parameters incorporated both survival and reproductive impacts. All impacts were modeled as 10% reductions in the affected population demographic parameters. First-year survival and reproductive impacts produced similar population growth rates (λ), but resulted in different sensitivity and stable age distributions. Modeled somatic growth reduction produced additive effects on survival and reproduction. Toxic stressors producing similar changes in λ did not necessarily produce similar changes in the age distributions. Sensitivity and elasticity analyses demonstrated that changes to the first-year survival rate produced the greatest per-unit effect on λ for each species. Alteration in abundance of mature females also strongly influenced λ. Differences observed between species showed that the number of reproductive ages and time to reproductive maturity were important components for population-level responses. These results emphasize the importance of linking toxicity responses at low concentrations to the demographic traits they affect, and help to highlight the toxicity tests that are more suitable for assessing impacts on the focal species. Additionally, life history modeling is a useful tool for developing testable hypotheses regarding impacts on specific populations as well as for conducting comparisons between populations.     

The demographic consequences of the cost of reproduction in ungulates

The cost of reproduction can generate covariation between demographic rates that can potentially influence demography and population dynamics in long-lived iteroparous species. However, there has been relatively little work linking the survival cost of reproduction and population dynamics. The apparent scarcity of information on this important link is potentially due to covariation between vital rates, which can substantially influence fluctuations in population size. In this paper we examine the opportunity for survival costs of reproduction to leave a dynamic signature using a simulation model based broadly on an ungulate life history. We find that an increase in the cost delays the onset of reproduction and reduces reproductive rates of young, but not of prime-age, females. Accordingly, the number of offspring produced declines and the interval between reproductive events increases among young females experiencing high cost. These effects are translated to an age structure skewed toward young ages and reduced population density. These results suggest that, by delaying reproduction when conditions deteriorate, females protect their survival during the critical first three years of life, after which the negative effect of reproduction on survival declines. Unless conditions for reproduction are severe, it is not profitable to delay reproduction beyond age 3 years due to the high risk of death before having a chance to reproduce. We also demonstrate that lack of adjustment of reproductive strategies to elevated levels of the cost of reproduction, for example due to rapid changes in environmental conditions, results in lower average density and longevity compared to females that have sufficient time to adjust to changes in the cost. This suggests that even moderate costs of reproduction may have a major negative effect on population dynamics of ungulates.     

Ecological success of the cladoceran <Emphasis Type="Italic">Penilia avirostris</Emphasis> in the marine environment: feeding performance,gross growth efficiencies and life history

Marine cladocerans are important contributors to the zooplankton community of tropical and temperate coastal ecosystems during the warmer months, when they show explosive population growth. Despite this fact, little information is available on their ecology compared with the extensive studies on their freshwater relatives. The main objective of this study was to determine the in situ feeding and growth rates, and life history parameters of Penilia avirostris in São Sebastião Bay (Brazil) during austral summer 2004, as a premise to understand the advantages of this cladoceran in oligotrophic waters. Culture development experiments, monitored for a period of 12 days, showed that maximum juvenile release occurred after 2 days, and that the development duration of a complete cohort was around 9 days. From bottle incubation grazing experiments, significant ingestion rates upon flagellates, ciliates, dinoflagellates and diatoms were detected. Flagellates were the most important contributors to P. avirostris diet (ca. 80%). P. avirostris ingested between 28 and 97% of its own carbon biomass per day (daily ration) and individual growth rates of this marine cladoceran (0.10–0.24 d^?1) increased with prey availability. The combination of ingestion rates of natural prey and growth rates provided gross growth efficiencies (GGE) of 15–53%, on a carbon basis. Our results suggest that P. avirostris has similar GGE to copepods, although at low food conditions the values for the marine cladocerans seems slightly higher. However, this characteristic alone does not explain the explosive growth and community dominance shown by P. avirostris. Therefore, other traits related to the reproductive biology of the species, such as short generation time, parthenogenetic reproduction, and continuous somatic growth, seems to be mostly responsible for the success of P. avirostris in many marine ecosystems during their seasonal occurrence.     

Relationship between larval and juvenile growth rates in two marine gastropods,Crepidula plana and C. fornicata

Previous studies on various marine mollusc species have shown that both larval and juvenile growth rates are substantially heritable, but few workers have examined the extent to which larval and juvenile growth rates covary. We examined the relationship between larval and juvenile growth rates in seven laboratory experiments conducted between 1986 and 1993, using the prosobranch gastropods Crepidula plana Say and C. fornicata (L.). In most experiments larvae were reared individually, measured twice nondestructively to determine larval grwoth rate, allowed or stimulated (daily 5-h exposure to 20 mM excess K⁺ in seawater) to metamophose, and then measured at least twice after metamorphosis to determine juvenile growth rates. Generally, there was no significant (p >0.10) relationship between larval and juvenile growth rates, suggesting that in these two species selection can act independently on the two stages of development. A positive correlation (p=0.007) between larval and juvenile growth rates was observed for C. fornicata in one experiment, but only for offspring from females maturing the most rapidly in laboratory culture. Even for these larvae, however, variation in larval growth rate explained<2% of the variation in juvenile growth rate, so that larval and juvenile growth rates are at most only weakly associated in this species.     

Fitting probability models to population dynamics data

Methods for modeling population dynamics in probability using the generalized point process approach are developed. The life history of these populations is such that seasonal reproduction occurs during a short time. Several models are developed and analyzed. Data about two species: colonial spiders (Stegodyphus dumicola) and a migratory bird (wood thrush, Hylocichla mustelina) are used to estimate model parameters with appropriate log maximum likelihood functions. For the spiders, the model is fitted to provide evolutionary feasible colony size based on maximum likelihood estimates of fecundity and survival data. For the migratory bird species, a maximum likelihood estimates are derived for the fecundity and survival rates of young and adult birds and immigration rate. The presented approach allows computation of quantities of interest such as probability of extinction and average time to extinction.     

All at sea: aquatic life modifies mate-recognition modalities in sea snakes (Emydocephalus annulatus, Hydrophiidae)

Alternative sensory modalities (e.g. vision, chemoreception) differ in the spatial scale, permanence and reliability of cues they provide to mate-searching males. Males of terrestrial snake species use chemoreception to locate females over large distances, but phylogenetic shifts to aquatic life render such cues unavailable. Do male sea snakes use alternative modalities for identifying potential sexual partners and if so, are the novel systems as effective for mate-finding as the ancestral ones? Observations and experiments show that free-ranging male turtle-headed sea snakes (Emydocephalus annulatus) in shallow-water reef habitats in New Caledonia use visual cues (including size, movement and color pattern) to assess whether snake-shaped objects are potential sexual partners. Skin lipids (pheromones) are important only after the male comes into physical contact with the stimulus. Visual cues provide unreliable information about potential mates, and function over short distances only (generally, <1 m). In consequence, mate-searching male snakes frequently failed to find nearby females, rarely managed to maintain contact with females they did find, and wasted time and energy investigating inappropriate stimuli (e.g. fishes, sea cucumbers, divers). The loss of effective pheromonal mate-location systems means that mate recognition by aquatic snakes functions over smaller distances than in their terrestrial relatives. Phylogenetic transitions among habitat types thus may directly modify central features of the mating system.     

Age and growth of Electrona antarctica (Pisces: Myctophidae), the dominant mesopelagic fish of the Southern Ocean

Numerically and in biomass, the lanternfish Electrona antarctica is the dominant fish in the vast pelagic region of the Southern Ocean bounded on the north by the Antarctic Convergence and in the south by the Antarctic continental shelf. It is an important krill predator, and in turn is important in the diets of flighted and swimming seabirds. Further, it is the southernmost and coldest-dwelling representative of the globally distributed fish family Myctophidae. The present study was undertaken to estimate the species' growth rate and average life span, to incorporate the information in a basic energy budget, and to compare the growth of E. antarctica with more northerly confamilials. Fishes were aged using primary growth increments that were resolved on sagittal otoliths using three sequential techniques: thin-section grinding and polishing, etching, and scanning electron microscopy (SEM). Based on increment width (0.8 to 1.2 μm), continuity, and previous studies on confamilials, the microincrements were assumed to be deposited on a daily basis. Montages of SEM photomicrographs were constructed for each sagitta to allow the daily rings to be counted over the entire life span of 31 individuals representing the entire size range of the species. Results suggest a larval stage of 30 to 47 d and a maximum life span of 3.5 yr, with females growing faster than males in the last 1.5 yr of life and reaching a larger maximum size. Construction of a simple energy budget using the best information available suggests that a surplus of energy is available to support the observed growth rates (0.05 to 0.07 mm d⁻¹). The results of the present study contrast markedly with previous estimates of an 8 to 11 yr maximum age for E. antarctica. These results provide important data addressing the ecology and population dynamics of the pelagic Antarctic ecosystem. E. antarctica is the end-member species in the continuum of vertically migrating myctophids that extend from the equator to the polar circle. Its growth rate is consonant with that of all other myctophid species examined using primary growth increments to determine age. The present study, in conjunction with earlier studies, suggests that growth rates of mesopelagic species are far higher than previously thought. Received: 12 September 1997 / Accepted: 25 July 1998     

The amphipod Corophium multisetosum (Corophiidae) in Ria de Aveiro (NW Portugal). I. Life history and aspects of reproductive biology

The population of Corophium multisetosum Stock, 1952 in Areão displayed a semiannual, iteroparous life history. Mean longevity was ～6?mo, with the estimated life span longer for overwintering individuals born in autumn than for individuals born in spring. Length-frequency data indicated that the length increment per moult is probably higher in males than females; however females moulted more frequently and achieved a larger body size. Preliminary growth rates were 100?μm?d^?1 for juveniles and 19 to 29?μm?d^?1 for mature females, with the lower values occurring during the winter. It was estimated that under favourable conditions females may attain reproductive size and mature within 1?mo. Although incubating females were present all year round, recruitment occurred in spring, almost ceased during the summer, peaked in autumn, and decreased again during the winter. Extreme temperatures and very low salinities during winter and summer may have deterred breeding, while moderate temperatures (15 to 20?°C) and salinities > 1?psu in spring and autumn were apparently favourable for reproduction. The unfavourable summer conditions constrained breeding and synchronised the timing of reproduction. In late-autumn and during the winter, as temperature decreased and brooding time increased, synchrony was progressively lost. Brood size varied as a function of embryonic developmental stage, size of incubating females, and season. The life-history pattern and reproductive features of C. multisetosum in Areão are closely related to temperature and salinity; other environmental conditions such as oxygen content of the water and food availability may also be relevant.     

Brood or broadcast? The adaptive significance of different reproductive strategies in the two intertidal sea stars Leptasterias hexactis and Pisaster ochraceus

This paper considers the adaptive significance of two different reproductive methods in two co-occurring, competing sea stars. The smaller (3 to 8 g mean wet weight) Leptasterias hexactis broods relatively few, large young in the winter, while the large (300 to 650 g mean wet weight) Pisaster ochraceus broadcasts relatively many, small eggs each spring. L. hexactis matures at a small size (2 g wet weight) in about 2 years, and P. ochraceus matures at a larger size (70 to 90 g wet weight) in about 5 years (Menge, 1974). As in many broadcasting asteroids, gonad and storage organ indices of P. ochraceus are inversely related over time, and maximum storage-organ index correlates with the summer feeding maximum (Mauzey, 1966). In contrast, both organ indices of L. hexactis and feeding increase and are positively correlated until early autumn, when feeding activity begins to decline. At this time the male gonad index continues to rise, and the storage-organ index drops. In contrast, both organ indices of females rise. Spawning occurs from November to January. Thereafter storage-organ indices decline in females, presumably because females draw upon energy reserves while brooding; storage-organ indices rise in males, presumably because males do not brood and can feed if food is available. The primary cause for the differences between annual reproductive cycles of P. ochraceus and L. hexactis is suggested to be patterns of food availability for the released young (planktonic food for the broadcasted young of P. ochraceus and benthic prey for the brooded young of L. hexactis. Estimates of pre-maturity survival and post-maturity longevity indicate that the probability of survival per individual of young P. ochraceus is vastly lower than that of L. hexactis. However, once mature, P. ochraceus has a much longer expected lifespan. Brooding is suggested to be a coadaptive consequence of competition-induced small size. Assuming planktonic mortality rates in this environment are roughly constant across broadcasting species, I suggest that a small broadcasting species could not produce enough offspring in its expected lifespan to replace itself. This hypothesis is partly supported by some simple simulations. Broadcasting is suggested to permit rapid location and utilization of spatially and temporally unpredictable, but highly desirable, resources by allowing rapid and widespread dispersal. Brooders presumably cannot disperse rapidly and must rely on more reliable, but perhaps less desirable, resources. Factors affecting reproductive patterns in marine invertebrates include (1) food availability for both adults and offspring, (2) planktonic mortality rates, (3) interactions between species and latitudinal changes in these factors, and (4) various physical factors. This paper suggests that competition and predation can have an important effect on the evolution of reproductive methods, a possibility heretofore largely ignored. Although several similar examples of co-occurring species' pairs which differ in reproductive method and size are available, the role of adult interactions is unknown in these examples.     

Female reproductive qualities affect male painted turtle (Chrysemys picta marginata) reproductive success

Male reproductive success (RS) in polygamous species with minimal social systems is often determined by the number of mates. However, because male RS is translated through females, the number of offspring sired can also be influenced by female qualities. Empirically sufficient data to document how tradeoffs between mate number and quality influence male RS are seldom available for long-lived, iteroparous species. We combined long-term life history data (1983–2006) on the E. S. George Reserve (ESGR, MI, USA) with parentage data from 155 clutches of 59 female painted turtles (Chrysemys picta marginata) of varying reproductive frequencies (2003–2006) to determine the relative contribution of female numbers and qualities on male RS. One previously documented trait of female painted turtles that can have substantial influences on male RS is repeat paternity through the use of stored sperm to fertilize over 95 % of within-year clutches. In addition, our study found that second-clutch producing female painted turtles on the ESGR have higher among-year reproductive frequencies than do first-clutch only females. Multiple paternity was detected in 14.1 % of clutches (min-max?=?6.1–30.0 % annually), and the number of mates of both sexes was low annually (males 1.0; females 1.2) and over 4 years (males 1.1; females 1.7). Among successful males, RS varied substantially (1–32 offspring) and was strongly influenced by the combination of female reproductive frequency and repeat paternity (>38 % among years), but not mate number. Low mate number for both sexes was unexpected in a species without complex mating behaviors or parental care.     

Physiological basis of extreme growth rate differences in the spat of oyster (Crassostrea gigas)

Juvenile oysters (Crassostrea gigas) (produced in November 2009) reared under uniform hatchery conditions for 4 months were selected for extreme growth rate differences by repeatedly taking larger and smaller individuals to achieve weight differences >30× between fast (F) and slow (S) growers. The physiological basis of differential growth was analyzed in experiments in June 2010, where components of energy gain (clearance and ingestion rates and absorption efficiency), energy loss (metabolic rates) and resulting scope for growth (J h^?1) were compared for groups of F and S oysters fed three different ration levels (≈0.5, 1.5 and 3.0 mg of total particulate matter L^?1). In both F and S oysters, a higher food ration promoted asymptotic increases in energy gain rates through regulatory adjustments to clearance rates, which maintained similar absorption efficiencies across the food concentrations. No significant differences were found between growth groups in mass-specific physiological rates (i.e., per unit of body mass). However, the scaling of these rates to a common size in both groups using allometric coefficients derived for C. gigas revealed higher energy gain rates coupled with lower metabolic costs of growth in fast growers. Thus, appropriate size-standardization is essential in accounting for observed differences in growth rate. Present results are in accordance with previous reports on other bivalve species on the physiological processes underlying endogenous growth differences, suggesting that the same interpretation can be applied to the extremes of these differences.     

Effects of autotomy on long-term survival and growth of painted spiny lobster (Panulirus versicolor) on the Great Barrier Reef, Australia

The effects of autotomy (shedding of appendages) on survival and growth rates of painted spiny lobster were investigated at Northwest Island (23^° 18?? S, 152^° 43?? E) during the period 2003?C2006. Adult lobsters were captured, tagged, and classified as either uninjured (n?=?68), minimally injured (n?=?39) or moderately injured (n?=?19) depending on the number and type of appendages that were autotomized during capture and handling. Six to thirty-six months after release, 86 lobsters were recaptured (mean time at large?=?305?days). Recapture rates of uninjured (64.7%), minimally injured (71.8%), and moderately injured lobsters (73.7%) were not significantly different. Similarly, mean annualized growth rates of uninjured, minimally injured, and moderately injured lobsters were not significantly different. This suggests that the energetic cost of a single episode of autotomy is either negligible or exists as a trade-off with some other life history trait, such as reduced reproductive performance. These results support the use of certain management tools (e.g., size limits) that prescribe release of non-legal lobsters, regardless of their injury status.     

Shiny cowbirds share foster mothers but not true mothers in multiply parasitized mockingbird nests

Obligate brood parasitic birds, such as cowbirds, evade parental care duties by laying their eggs in the nests of other species. Cowbirds are assumed to avoid laying repeatedly in the same nest so as to prevent intrabrood competition between their offspring. However, because searching for host nests requires time and energy, laying more than one egg per nest might be favoured where hosts are large and can readily rear multiple parasites per brood. Such ‘repeat parasitism’ by females would have important consequences for parasite evolution because young parasites would then incur indirect fitness costs from behaving selfishly. We investigated shiny cowbird (Molothrus bonariensis) parasitism of a large host, the chalk-browed mockingbird (Mimus saturninus), in a population where over 70 % of the parasitized mockingbird nests receive multiple cowbird eggs. We assessed egg maternity directly, using cameras at nests to film the laying of individually-marked females. We also supplemented video data with evidence from egg morphology, after confirming that each female lays eggs of a consistent appearance. From 133 eggs laid, we found that less than 5 % were followed by the same female visiting the nest to lay again or to puncture eggs. Multiple eggs in mockingbird nests were instead the result of different females, with up to eight individuals parasitizing a single brood. Thus, while cowbird chicks regularly share mockingbird nests with conspecifics, these are unlikely to be their maternal siblings. Our results are consistent with shiny cowbird females following a one-egg-per-nest rule, even where hosts can rear multiple parasitic young.     

Activation energy for skeletal aragonite deposited by the hermatypic coral Platygyra spp.

Average radial growth rates of the hemispherical aragonite colonies deposited by the Indo-Pacific scleractinian reef coral Platygyra spp. were determined by measuring the thickness of density variations in the skeleton that are revealed by X-radiography. Ninety-one specimens from 21 localities were examined, but only 54 of these exhibited well-defined growth-banding. The apparent temperature dependence of growth rate is linear over the range 23.9° to 29.3°C, averaging 5.4±0.94 mm/year at 24°C, 8.0±0.42 mm/year at 27°C, and 9.7 ±0.58 mm/year at 29°C (90% confidence limits). Expression of the influence of temperature on growth rate in terms of the Arrhenius equation yields an activation energy of 20,680 cal/mole, which is comparable to values for typical biological reactions, but is only half that reported for skeletogenesis in another reef coral, Pocillopora damicornis, on the basis of controlled incubation studies involving ⁴⁵Ca uptake.     

Sex differences in the ontogeny of social behavior in pikas: possible relationships to dispersal and territoriality

Summary A laboratory study on the ontogeny of social behavior in pikas (Ochotona princeps), an alpine lagomorph, was conducted to determine the role of early relationships between adult females and young and among siblings in the development of territorial and dispersal behaviors. Sex differences during development were examined because field studies have reported greater dispersal distances in young females than young males. At birth, females were significantly heavier than males. There were no sex differences in nursing frequency until after the 2nd week of age, when males initiated more nursing attempts than females. By the end of the weaning period (weeks 5 and 6), adult females became non-interactive with young, but aggression of young toward littermates and the mother increased until the eighth week. At this time, young males outweighed their sibling females. Young were dominant over their mothers by the age of 5 weeks, and young males were dominant over their sibling females.Sex differences were observed in aggression, scent-marking, exploratory activity, and submissive vocalizations, with higher rates in young males, except for submissive vocalizations, which were higher in females (Table 2). Vocalizations and scent-marking behavior increased over time, and were positively correlated with interaction rates.These data support the hypothesis that female young disperse farther than male young largely as the result of unsuccessful competition with male siblings for available territories close to the birthplance. A dispersal strategy for pkkas is proposed.     

Life History as a Predictor of Salamander Recovery Rate from Timber Harvest in Southern Appalachian Forests,U.S.A

Forest management often represents a balance between social, economic, and ecological objectives. In the eastern United States, numerous studies have established that terrestrial salamander populations initially decline in abundance following timber harvest, yet the large‐scale and long‐term consequences are relatively unknown. We used count data from terrestrial survey points to examine the relation between salamander abundance and historic timber harvest while accounting for imperfect detection of individuals. Overall, stream‐ and terrestrial‐breeding salamanders appeared to differ by magnitude of population decline, rate of population recovery, and extent of recolonization from surrounding forest. Specifically, estimated abundance of both species groups was positively associated with stand age and recovery rates were predicted to increase over time for red‐legged salamanders (Plethodon shermani) and decrease in stream‐breeding species. Abundance of stream‐breeding salamanders was predicted to reach a peak by 100 years after timber harvest, and the population growth rate of red‐legged salamanders was predicted to undergo a significant increase 100 years after harvest. Estimated abundance of stream‐breeding salamanders in young forest stands was also negatively associated with the distance to adjacent forest, a result that suggests immigration has a role in the recovery of these species. Our results indicate that salamander abundance in young forest stands may be only modestly lower than in more mature forest but that full recovery from timber harvest may take a substantial amount of time and that species life history may affect patterns of recovery. Historia de Vida como un Vaticinador de la Tasa de Recuperación de una Salamandra a la Colecta de Madera en los Bosques del Sur de los Apalaches, E.U.A     

Life history consequences of variation in age at primiparity in northern elephant seals

Summary The age when female northern elephant seals, Mirounga angustirostris, bear their first young varies from 2 to 6 years. At Año Nuevo, California, a group of 77 females, primiparous at age 3, had a lower survivorship rate to each successive year up to age 8 than a group of 98 females that deferred initial pupping until age 4. The difference in survivorship appears to be due to the greater relative energetic costs of gestation and lactation incurred by the earlier breeding females during a period in their development when growth is rapid. An alternate hypothesis for the difference in survivorship — that young primiparous females are in poor condition from birth-is untenable; females that pupped early in life were larger at weaning age (a correlate of condition) than females that were primiparous 1 year later.Models based on the data show that differential survival of seals that vary in age at primiparity has important consequences for population growth and life history strategies. The effect of age at primiparity on the rate of increase of populations varies with colony density and juvenile survivorship. The optimal life history strategy for female elephant seals under most conditions existing today, including those at Ano Nuevo during the study period, is to bear the first offspring at age 4. Primiparity at age 3 is projected to be favored when harem density is very low and weaning success and juvenile survivorship are high; postponement of first breeding to age 5 is expected at high harem densities with intense competition for breeding space. Offprint requests to: B.J. Le Boeuf