From plankton to top predators: bottom-up control of a marine food web across four trophic levels

1. Abundant mid-trophic pelagic fish often play a central role in marine ecosystems, both as links between zooplankton and top predators and as important fishery targets. In the North Sea, the lesser sandeel occupies this position, being the main prey of many bird, mammal and fish predators and the target of a major industrial fishery. However, since 2003, sandeel landings have decreased by > 50%, and many sandeel-dependent seabirds experienced breeding failures in 2004. 2. Despite the major economic implications, current understanding of the regulation of key constituents of this ecosystem is poor. Sandeel abundance may be regulated 'bottom-up' by food abundance, often thought to be under climatic control, or 'top-down' by natural or fishery predation. We tested predictions from these two hypotheses by combining unique long-term data sets (1973–2003) on seabird breeding productivity from the Isle of May, SE Scotland, and plankton and fish larvae from the Continuous Plankton Recorder survey. We also tested whether seabird breeding productivity was more tightly linked to sandeel biomass or quality (size) of individual fish. 3. The biomass of larval sandeels increased two- to threefold over the study period and was positively associated with proxies of the abundance of their plankton prey. Breeding productivity of four seabirds bringing multiple prey items to their offspring was positively related to sandeel larval biomass with a 1-year lag, indicating dependence on 1-year-old fish, but in one species bringing individual fish it was strongly associated with the size of adult sandeels. 4. These links are consistent with bottom-up ecosystem regulation and, with evidence from previous studies, indicate how climate-driven changes in plankton communities can affect top predators and potentially human fisheries through the dynamics of key mid-trophic fish. However, the failing recruitment to adult sandeel stocks and the exceptionally low seabird breeding productivity in 2004 were not associated with low sandeel larval biomass in 2003, so other mechanisms (e.g. predation, lack of suitable food after metamorphosis) must have been important in this case. Understanding ecosystem regulation is extremely important for predicting the fate of keystone species, such as sandeels, and their predators.

The application of randomly amplified polymorphic DNA (RAPD's) to the study of Lasaea rubra (Montagu).

This paper describes the random amplification of polymorphic DNA markers (RAPDs) in Lasaea rubra (Erycinidae: Bivalvia). Present evidence suggests that L. rubra is an asexual species; however, the exact mode of clonal reproduction in this species is still a matter of debate. In this preliminary study, four of the primers used generated polymorphic RAPDs. One primer was able to distinguish between individuals from the same or different crevice population. This same primer also resolved a single band difference between otherwise identical RAPD patterns of a parent and its offspring. No familial differences have been detected in several previous studies using allozyme electrophoresis. This paper suggests that many polymorphic markers could be obtained with this species using the RAPD technique. Population genetic analysis of L. rubra has long been hampered by a dearth of polymorphic markers due to its small size. These findings suggest that this technique has the potential to further the study of population genetics in this asexual species.

Differential lifetime success and performance of native and non-native Atlantic salmon examined under communal natural conditions.

The lifetime success and performance characteristics of communally reared offspring of wild native Burrishoole (native), ranched native (ranched) and non-native (non-native) Atlantic salmon Salmo salar from the adjacent Owenmore River were compared. Non-native year parr showed a substantial downstream migration, which was not shown by native and ranched parr. This appears to have been an active migration rather than competitive displacement and may reflect an adaptation to environmental or physiographic conditions within the Owenmore River catchment where the main nursery habitat is downstream of the spawning area. There were no differences between native and ranched in smolt output or adult return. Both of these measures, however, were significantly lower for the non-native group. A greater proportion of the non-native Atlantic salmon was taken in the coastal drift nets compared to the return to the Burrishoole system, probably as a result of the greater size of the non-native fish. The overall lifetime success of the non-native group, from fertilized egg to returning adult, was some 35% of native and ranched. The ranched group showed a significantly greater male parr maturity, a greater proportion of 1+ year smolts, and differences in sex ratio and timing of freshwater entry of returning adults compared to native, which may have fitness implications under specific conditions.

Fitness reduction and potential extinction of wild populations of Atlantic salmon, Salmo salar, as a result of interactions with escaped farm salmon.

The high level of escapes from Atlantic salmon farms, up to two million fishes per year in the North Atlantic, has raised concern about the potential impact on wild populations. We report on a twogeneration experiment examining the estimated lifetime successes, relative to wild natives, of farm, F1 and F2 hybrids and BC1 backcrosses to wild and farm salmon. Offspring of farm and hybrids (i.e. all F1 , F2 and BC1 groups) showed reduced survival compared with wild salmon but grew faster as juveniles and displaced wild parr, which as a group were significantly smaller. Where suitable habitat for these emigrant parr is absent, this competition would result in reduced wild smolt production. In the experimental conditions, where emigrants survived downstream, the relative estimated lifetime success ranged from 2% (farm) to 89% (BC1 wild) of that of wild salmon, indicating additive genetic variation for survival . Wild salmon primarily returned to fresh water after one sea winter (1SW) but farm and hybrids produced proportionately more 2SW salmon. However, lower overall survival means that this would result in reduced recruitment despite increased 2SW fecundity. We thus demonstrate that interaction of farm with wild salmon results in lowered fitness, with repeated escapes causing cumulative fitness depression and potentially an extinction vortex in vulnerable populations.

Correlates of reproductive success in a population of nine-banded armadillos: a preliminary report.

We used microsatellite DNA markers to identify the putative parents of 69 litters of nine-banded armadillos (Dasypus novemcinctus) over 4 years. Male and female parents did not differ in any measure of body size in comparisons with nonparents. However, males observed paired with a female were significantly larger than unpaired males, although paired females were the same size as unpaired females. Females categorized as possibly lactating were significantly larger than females that were either definitely lactating or definitely not lactating. There was no evidence of assortative mating: body-size measurements of mothers were not significantly correlated with those of fathers. Nine-banded armadillos give birth to litters of genetically identical quadruplets. Mothers (but not fathers) of female litters were significantly larger than mothers of male litters, and maternal (but not paternal) body size was positively correlated with the number of surviving young within years, but not cumulatively. There were no differences in dates of birth between male and female litters, nor were there any significant relationships between birth date and maternal body size. Body size of either parent was not correlated with the body sizes of their offspring. Cumulative and yearly reproductive success did not differ between reproductively successful males and females. Average reproductive success (which included apparently unsuccessful individuals) also did not differ between males and females. The majority of adults in the population apparently failed to produce any surviving offspring, and even those that did usually did so in only 1 of the 4 years. This low reproductive success is unexpected, given the rapid and successful range extension of this species throughout the southeastern United States in this century.

The adaptive value of polyembryony.

From an evolutionary standpoint, the production of offspring is the single most important aspect of an animal's life. Offspring carry an individual's genes into the next generation and it is the differential representation of genes in a population that drives evolutionary change. There are a variety of ways in which animals create offspring, ranging from cases where parents make identical copies of themselves by budding or parthenogenesis, to the standard case in vertebrates where gametes from a male and female fuse in sexual reproduction to produce the next generation. In this article we describe an usual variant of sexual reproduction, polyembryony.

Genetic maternity and paternity in a local population of armadillos assessed by microsatellite DNA markers and field data.

Genetic data from polymorphic microsatellite loci were employed to estimate paternity and maternity in a local population of nine-banded armadillos (Dasypus novemcinctus) in northern Florida. The parentage assessments took advantage of maximum likelihood procedures developed expressly for situations when individuals of neither gender can be excluded a priori as candidate parents. The molecular data for 290 individuals, interpreted alone and in conjunction with detailed biological and spatial information for the population, demonstrate high exclusion probabilities and reasonably strong likelihoods of genetic parentage assignment in many cases; low mean probabilities of successful reproductive contribution to the local population by individual armadillo adults in a given year; and statistically significant microspatial associations of parents and their offspring. Results suggest that molecular assays of highly polymorphic genetic systems can add considerable power to assessments of biological parentage in natural populations even when neither parent is otherwise known.

How optimal life history changes with the community size-spectrum

This paper derives optimal life histories for fishes or other animals in relation to the size spectrum of the ecological community in which they are both predators and prey. Assuming log-linear size-spectra and well known scaling laws for feeding and mortality, we first construct the energetics of the individual. From these we find, using dynamic programming, the optimal allocation of energy between growth and reproduction as well as the trade-off between offspring size and numbers. Optimal strategies were found to be strongly dependent on size spectrum slope. For steep size spectra (numbers declining rapidly with size), determinate growth was optimal and allocation to somatic growth increased rapidly with increasing slope. However, restricting reproduction to a fixed mating season changed optimal allocations to give indeterminate growth approximating a von Bertalanffy trajectory. The optimal offspring size was as small as possible given other restrictions such as newborn starvation mortality. For shallow size spectra, finite optimal maturity size required a decline in fitness for large size or age. All the results are compared with observed size spectra of fish communities to show their consistency and relevance.

Queen-worker conflict over male production and sex ratio in a facultatively polyandrous bumble bee, Bombus hypnorum: the consequences of nest usurpation.

Evolutionary conflicts among social hymenopteran nestmates are theoretically likely to arise over the production of males and the sex ratio. Analysis of these conflicts has become an important focus of research into the role of kin selection in shaping social traits of hymenopteran colonies. We employ microsatellite analysis of nestmates of one social hymenopteran, the primitively eusocial and monogynous bumblebee Bombus hypnorum, to evaluate these conflicts. In our 14 study colonies, B. hypnorum queens mated between one and six times (arithmetic mean 2.5). One male generally predominated, fathering most of the offspring, thus the effective number of matings was substantially lower (1–3.13; harmonic mean 1.26). In addition, microsatellite analysis allowed the detection of alien workers, those who could not have been the offspring of the queen, in approximately half the colonies. Alien workers within the same colony were probably sisters. Polyandry and alien workers resulted in high variation among colonies in their sociogenetic organization. Genetic data were consistent with the view that all males (n = 233 examined) were produced by a colony’s queen. Male parentage was therefore independent of the sociogenetic organization of the colony, suggesting that the queen, and not the workers, was in control of the laying of male-destined eggs. The population-wide sex ratio (fresh weight investment ratio) was weakly female biased. No evidence for colony-level adaptive sex ratio biasing could be detected.

Interleukin 18 promoter polymorphisms are not strongly associated with type 1 diabetes in a UK population

Interleukin 18 (IL18) is a proinflammatory cytokine whose levels are increased in the subclinical stage of insulin-dependent (type I) diabetes mellitus. Previous case-control studies have reported associations between IL18 -607C>A and -137G>C promoter polymorphisms and type I diabetes. We performed case-control and family-based association studies employing Pyrosequencing to assess if these IL18 polymorphisms are also associated with the development of type I diabetes in the Northern Ireland population. The chi2 analysis of genotype and allele frequencies for the IL18 polymorphisms in cases (n=433) vs controls (n=426) revealed no significant differences (P>0.05). Assessment of allele transmission distortion from informative parents to affected offspring also failed to confirm previously reported associations. Stratification of these analyses for age-at-onset and HLA-DR type did not reveal any significance associations. In conclusion, our data do not support the strong positive associations of IL18 promoter polymorphisms with type I diabetes reported in previous smaller studies.

Is big best? Queen size, usurpation and nest closure in a primitively eusocial sweat bee (Lasioglossum malachurum).

For primitively eusocial insects in which a single foundress establishes a nest at the start of the colony cycle, the solitary provisioning phase before first worker emergence represents a risky period when other, nestless foundresses may attempt to usurp the nest. In the primitively eusocial sweat bee Lasioglossum malachurum (Hymenoptera, Halictidae), spring foundresses compete for nests which are dug into hard soil. Nest-searching foundresses (‘floaters’) frequently inspected nests during this solitary phase and thereby exerted a usurpation pressure on resident queens. Usurpation has been hypothesised to increase across the solitary provisioning phase and favour closure of nests at an aggregation, marking the termination of the solitary provisioning phase by foundresses, before worker emergence. However, our experimental and observational data suggest that usurpation pressure may remain constant or even decrease across the solitary provisioning phase and therefore cannot explain nest closure before first worker emergence. Levels of aggression during encounters between residents and floaters were surprisingly low (9% of encounters across 2 years), and the outcome of confrontations was in favour of residents (resident maintains residency in 94% of encounters across 2 years). Residents were significantly larger than floaters. However, the relationship between queen size and offspring production, though positive, was not statistically significant. Size therefore seems to confer a considerable advantage to a queen during the solitary provisioning phase in terms of nest residency, but its importance in terms of worker production appears marginal. Factors other than intraspecific usurpation need to be invoked to explain the break in provisioning activity of a foundress before first worker emergence.

Do protected areas mitigate the effects of fisheries-induced evolution on parental care behaviour of a recreationally-important teleost fish?

Human-induced selection on animals and plants has been highly influential throughout our history and resulted in both intentional benefits and unintended detriments. Fisheries-induced evolution (FIE) describes the unintended selection on wild fish populations by fishing that has resulted in the evolution of exploited populations. While the use of aquatic protected areas that exclude angling might be considered an evolutionarily-enlightened management approach to dealing with issues arising from FIE little is known about the effectiveness of this approach for maintaining the phenotypic diversity of traits in protected areas versus those outside of their boundaries. In species that exhibit parental care, including the largemouth bass (Micropterus salmoides), active nest guarding and aggression towards potential brood predators by males increases the survival of offspring. This aggression may render these individuals particularly vulnerable to capture via angling as a result of increased propensity to attack fishing lures near their nests. Relative levels of aggression by these males during the parental care period correlate with their vulnerability to angling year round. Inasmuch as this parental behavior is heritable, this selective removal of more aggressive individuals by anglers should drive population-average phenotypes towards lower levels of aggression. To assess the effectiveness of protected areas at mitigating FIE, I compared the nest guarding behaviours of wild, free-swimming male bass during the early nesting period for bass within and outside protected areas. I found that nesting males within long-standing fishing sanctuaries (>70 yrs) were more aggressive towards captive bluegill sunfish (Lepomis macrochirus) placed directly on their nests, and patrolled larger areas around their nests compared to bass outside of sanctuaries. Males within protected areas were more likely to strike at artificial fishing lures and more prone to capture during experimental angling events. Collectively, my findings suggest that recreational angling selects for individual bass with lower levels of parental care and aggression, and that the establishment of protected areas may mitigate potential FIE. The extent to which this phenomenon occurs in other species and systems likely depends on the reproductive strategies of the fishes being considered, their spatial ecology relative to sanctuary boundaries, and habitat quality within protected areas.

Testing the possible negative association of type 1 diabetes and atopic disease by analysis of the interleukin 4 receptor gene

Variations in the interleukin 4 receptor A (IL4RA) gene have been reported to be associated with atopy, asthma, and allergy, which may occur less frequently in subjects with type 1 diabetes (T1D). Since atopy shows a humoral immune reactivity pattern, and T1D results from a cellular (T lymphocyte) response, we hypothesised that alleles predisposing to atopy could be protective for T1D and transmitted less often than the expected 50% from heterozygous parents to offspring with T1D. We genotyped seven exonic single nucleotide polymorphisms (SNPs) and the -3223 C>T SNP in the putative promoter region of IL4RA in up to 3475 T1D families, including 1244 Finnish T1D families. Only the -3223 C>T SNP showed evidence of negative association (P=0.014). There was some evidence for an interaction between -3233 C>T and the T1D locus IDDM2 in the insulin gene region (P=0.001 in the combined and P=0.02 in the Finnish data set). We, therefore, cannot rule out a genetic effect of IL4RA in T1D, but it is not a major one.

Parent-off spring associations in wintering brent geese: parental investment or mutual assistance?

The continued parent-offspring associations in the Eastern Canadian High Arctic light-bellied brent goose Branta bernicla hrota was examined to determine whether this is an example of continued parental investment or mutual assistance. Adults with juveniles spend more than twice as much time being vigilant and aggressive than do those without offspring. The loss of a partner, however, does not result in the remaining parent increasing parental care but does result in increased 'self-care' by the juveniles. Neither parents nor single-parent juveniles appear to pay an energetic cost relative to non-parental adults and two-parent juveniles, respectively. Differences in the feeding distribution of parents and non-parents and equivalent or better physical condition suggests that families are able to maintain access to a superior food supply over the winter. Passive 'assistance' by juveniles may assist in maintaining this position in favoured areas, and this is achieved with little overt aggression. The present study thus provides no data that show a net cost to parents by remaining with their juveniles over the winter period. Thus, mutual assistance might be a better explanation of the prolonged association rather than a period of parental investment with an overall cost.

Shared or unshared parental care in overwintering brent geese (Branta bernicla hrota)

We examine brood size effects on the behaviour of wintering parent and juvenile brent geese (Branta bernicla hrota) to test predictions of shared and unshared parental care models. The behaviour of both parents and offspring appear to be influenced by declining food availability over the winter. Parental vigilance increased with brood size and may be explained by vigilance having functions in addition to antipredator behaviour where the benefits are shared among the brood. There was no increase in parental aggression with brood size and this does not fit the prediction of shared care. Nevertheless, large families are able to monopolize better feeding areas compared with smaller families and large families static feed more but walk feed less than do small families, the former apparently being the preferred mode. The presence of additional young, rather than increasing the amount of parental aggression, seems to enhance the family's competitive ability. Because parents with large broods benefit from enhanced access to resources there is likely to be no additional significant cost in the parental care of larger broods (sensu Trivers 1972).