Spatial distribution of selenium-mercury in Arctic seabirds.

Mercury (Hg) is a metallic trace element toxic for humans and wildlife that can originate from natural and anthropic sources. Hg spatial gradients have been found in seabirds from the Arctic and other oceans, suggesting contrasting toxicity risks across regions. Selenium (Se) plays a protective role against Hg toxicity, but its spatial distribution has been much less investigated than that of Hg. From 2015 to 2017, we measured spatial co-exposure of Hg and Se in blood samples of two seabird species, the Brünnich's guillemot (Uria lomvia) and the black-legged kittiwake (Rissa tridactyla) from 17 colonies in the Arctic and subarctic regions, and we calculated their molar ratios (Se:Hg), as a measure of Hg sequestration by Se and, therefore, of Hg exposure risk. We also evaluated concentration differences between species and ocean basins (Pacific-Arctic and Atlantic-Arctic), and examined the influence of trophic ecology on Hg and Se concentrations using nitrogen and carbon stable isotopes. In the Atlantic-Arctic ocean, we found a negative west-to-east gradient of Hg and Se for guillemots, and a positive west-to-east gradient of Se for kittiwakes, suggesting that these species are better protected from Hg toxicity in the European Arctic. Differences in Se gradients between species suggest that they do not follow environmental Se spatial variations. This, together with the absence of a general pattern for isotopes influence on trace element concentrations, could be due to foraging ecology differences between species. In both oceans, the two species showed similar Hg concentrations, but guillemots showed lower Se concentrations and Se:Hg than kittiwakes, suggesting a higher Hg toxicity risk in guillemots. Within species, neither Hg, nor Se or Se:Hg differed between both oceans. Our study highlights the importance of considering Se together with Hg, along with different species and regions, when evaluating Hg toxic effects on marine predators in international monitoring programs.

Mercury contamination and potential health risks to Arctic seabirds and shorebirds.

Since the last Arctic Monitoring and Assessment Programme (AMAP) effort to review biological effects of mercury (Hg) on Arctic biota in 2011 and 2018, there has been a considerable number of new Arctic bird studies. This review article provides contemporary Hg exposure and potential health risk for 36 Arctic seabird and shorebird species, representing a larger portion of the Arctic than during previous AMAP assessments now also including parts of the Russian Arctic. To assess risk to birds, we used Hg toxicity benchmarks established for blood and converted to egg, liver, and feather tissues. Several Arctic seabird populations showed Hg concentrations that exceeded toxicity benchmarks, with 50 % of individual birds exceeding the "no adverse health effect" level. In particular, 5 % of all studied birds were considered to be at moderate or higher risk to Hg toxicity. However, most seabirds (95 %) were generally at lower risk to Hg toxicity. The highest Hg contamination was observed in seabirds breeding in the western Atlantic and Pacific Oceans. Most Arctic shorebirds exhibited low Hg concentrations, with approximately 45 % of individuals categorized at no risk, 2.5 % at high risk category, and no individual at severe risk. Although the majority Arctic-breeding seabirds and shorebirds appeared at lower risk to Hg toxicity, recent studies have reported deleterious effects of Hg on some pituitary hormones, genotoxicity, and reproductive performance. Adult survival appeared unaffected by Hg exposure, although long-term banding studies incorporating Hg are still limited. Although Hg contamination across the Arctic is considered low for most bird species, Hg in combination with other stressors, including other contaminants, diseases, parasites, and climate change, may still cause adverse effects. Future investigations on the global impact of Hg on Arctic birds should be conducted within a multi-stressor framework. This information helps to address Article 22 (Effectiveness Evaluation) of the Minamata Convention on Mercury as a global pollutant.

Telomere lengths correlate with fitness but assortative mating by telomeres confers no benefit to fledgling recruitment.

Assortative mating by telomere lengths has been observed in several bird species, and in some cases may increase fitness of individuals. Here we examined the relationship between telomere lengths of Blue-footed Booby (Sula nebouxii) mates, long-lived colonial seabirds with high annual divorce rates. We tested the hypothesis that interactions between maternal and paternal telomere lengths affect offspring and parental survival. We found that relative telomere lengths (RTL) were strongly positively correlated between members of a breeding pair. In addition, RTL of both parents interacted to predict fledgling recruitment, although fledglings with two very long-RTL parents performed only averagely. Telomere lengths also predicted adult survival: birds with long telomeres were more likely to survive, but birds whose mate had long telomeres were less likely to survive. Thus, having long telomeres benefits survival, while choosing a mate with long telomeres benefits reproductive output while penalizing survival. These patterns demonstrate that while a breeder's RTL predicts offspring quality, assortative mating by RTL does not enhance fitness, and a trade-off between different components of fitness may govern patterns of assortative mating by telomere length. They also illustrate how testing the adaptive value of only one parent's telomere length on either survival or reproductive success alone may provide equivocal results.

Wintering in the Western Subarctic Pacific Increases Mercury Contamination of Red-Legged Kittiwakes.

Marine methylmercury concentrations vary geographically and with depth, exposing organisms to different mercury levels in different habitats. Red-legged kittiwakes (Rissa brevirostris), a specialist predator, forage on fish and invertebrates from the mesopelagic zone, a part of the ocean with elevated methylmercury concentrations. We used kittiwakes as bioindicators of MeHg concentrations in remote mesopelagic systems by examining how wintering distribution and habitat affected kittiwakes' mercury exposure. In 2011-2017, we sampled winter-grown feathers on St. George Island, Alaska, from birds equipped with geolocation loggers. We measured total mercury (THg) and nitrogen stable isotopes in nape and head feathers grown during winter, respectively. THg concentration of kittiwake nape feathers averaged 4.61 ± 0.97 µg/g dry weight. Hierarchical cluster analysis was used to classify winter habitats with remotely sensed environmental variables along each bird's track. Five habitat clusters were identified. Birds that spent more time in the Western Subarctic Gyre and those that wintered further south had elevated THg concentrations. In contrast to THg, trophic level varied annually but did not show strong spatial patterns. Our results documented spatial variability in THg exposure based on the oceanic wintering locations of red-legged kittiwakes and highlight their use as a bioindicator of MeHg across ocean basins.

Tissue-specific telomere dynamics in hibernating arctic ground squirrels (Urocitellus parryii).

Hibernation is used by a variety of mammals to survive seasonal periods of resource scarcity. Reactive oxygen species (ROS) released during periodic rewarming throughout hibernation, however, may induce oxidative damage in some tissues. Telomeres, which are the terminal sequences of linear chromosomes, may shorten in the presence of ROS, and thus the telomere length of an individual reflects the degree of accrued oxidative damage. This study quantified telomere length dynamics throughout hibernation in arctic ground squirrels (Urocitellus parryii). We hypothesized that telomere dynamics are tissue specific and predicted that telomere shortening would be most pronounced in brown adipose tissue (BAT), the organ that directly supports non-shivering thermogenesis during arousals. We used qPCR to determine relative telomere length (RTL) in DNA extracted from liver, heart, skeletal muscle (SM) and BAT of 45 juvenile and adult animals sampled either at mid- or late hibernation. Age did not have a significant effect on RTL in any tissue. At mid-hibernation, RTL of juvenile females was longer in BAT and SM than in liver and heart. In juvenile females, RTL in BAT and SM, but not in liver and heart, was shorter at late hibernation than at mid-hibernation. At late hibernation, juvenile males had longer RTL in BAT than did juvenile females, perhaps due to the naturally shorter hibernation duration of male arctic ground squirrels. Finally, BAT RTL at late hibernation negatively correlated with arousal frequency. Overall, our results suggest that, in a hibernating mammal, telomere shortening is tissue specific and that metabolically active tissues might incur higher levels of molecular damage.

The rate of telomere loss is related to maximum lifespan in birds.

Telomeres are highly conserved regions of DNA that protect the ends of linear chromosomes. The loss of telomeres can signal an irreversible change to a cell's state, including cellular senescence. Senescent cells no longer divide and can damage nearby healthy cells, thus potentially placing them at the crossroads of cancer and ageing. While the epidemiology, cellular and molecular biology of telomeres are well studied, a newer field exploring telomere biology in the context of ecology and evolution is just emerging. With work to date focusing on how telomere shortening relates to individual mortality, less is known about how telomeres relate to ageing rates across species. Here, we investigated telomere length in cross-sectional samples from 19 bird species to determine how rates of telomere loss relate to interspecific variation in maximum lifespan. We found that bird species with longer lifespans lose fewer telomeric repeats each year compared with species with shorter lifespans. In addition, phylogenetic analysis revealed that the rate of telomere loss is evolutionarily conserved within bird families. This suggests that the physiological causes of telomere shortening, or the ability to maintain telomeres, are features that may be responsible for, or co-evolved with, different lifespans observed across species.This article is part of the theme issue 'Understanding diversity in telomere dynamics'.

Effects of developmental conditions on growth, stress and telomeres in black-legged kittiwake chicks.

Early-life conditions can drive ageing patterns and life history strategies throughout the lifespan. Certain social, genetic and nutritional developmental conditions are more likely to produce high-quality offspring: those with good likelihood of recruitment and productivity. Here, we call such conditions "favoured states" and explore their relationship with physiological variables during development in a long-lived seabird, the black-legged kittiwake (Rissa tridactyla). Two favoured states were experimentally generated by manipulation of food availability and brood size, while hatching order and sex were also explored as naturally generating favoured states. Thus, the favoured states we explored were high food availability, lower levels of sibling competition, hatching first and male sex. We tested the effects of favoured developmental conditions on growth, stress, telomere length (a molecular marker associated with lifespan) and nestling survival. Generation of favoured states through manipulation of both the nutritional and social environments furthered our understanding of their relative contributions to development and phenotype: increased food availability led to larger body size, reduced stress and higher antioxidant status, while lower sibling competition (social environment) led to lower telomere loss and longer telomere lengths in fledglings. Telomere length predicted nestling survival, and wing growth was also positively correlated with telomere length, supporting the idea that telomeres may indicate individual quality, mediated by favoured states.

A supergene determines highly divergent male reproductive morphs in the ruff.

Three strikingly different alternative male mating morphs (aggressive 'independents', semicooperative 'satellites' and female-mimic 'faeders') coexist as a balanced polymorphism in the ruff, Philomachus pugnax, a lek-breeding wading bird. Major differences in body size, ornamentation, and aggressive and mating behaviors are inherited as an autosomal polymorphism. We show that development into satellites and faeders is determined by a supergene consisting of divergent alternative, dominant and non-recombining haplotypes of an inversion on chromosome 11, which contains 125 predicted genes. Independents are homozygous for the ancestral sequence. One breakpoint of the inversion disrupts the essential CENP-N gene (encoding centromere protein N), and pedigree analysis confirms the lethality of homozygosity for the inversion. We describe new differences in behavior, testis size and steroid metabolism among morphs and identify polymorphic genes within the inversion that are likely to contribute to the differences among morphs in reproductive traits.

The jellyfish buffet: jellyfish enhance seabird foraging opportunities by concentrating prey.

High levels of jellyfish biomass have been reported in marine ecosystems around the world, but understanding of their ecological role remains in its infancy. Jellyfish are generally thought to have indirect negative impacts on higher trophic-level predators, through changes in lower trophic pathways. However, high densities of jellyfish in the water column may affect the foraging behaviour of marine predators more directly, and the effects may not always be negative. Here, we present novel observations of a diving seabird, the thick-billed murre, feeding on fish aggregating among the long tentacles of large jellyfish, by using small video loggers attached to the birds. We show that the birds encountered large jellyfish, Chrysaora melanaster, during most of their dives, commonly fed on fish associated with jellyfish, and appeared to specifically target jellyfish with a high number of fish aggregating in their tentacles, suggesting the use of jellyfish may provide significant energetic benefits to foraging murres. We conclude that jellyfish provide feeding opportunities for diving seabirds by concentrating forage fish, and that the impacts of jellyfish on marine ecosystems are more complex than previously anticipated and may be beneficial to seabirds.

Carry-over effects of food supplementation on recruitment and breeding performance of long-lived seabirds.

Supplementation of food to wild animals is extensively applied as a conservation tool to increase local production of young. However, in long-lived migratory animals, the carry-over effects of food supplementation early in life on the subsequent recruitment of individuals into natal populations and their lifetime reproductive success are largely unknown. We examine how experimental food supplementation early in life affects: (i) recruitment as breeders of kittiwakes Rissa tridactyla born in a colony on Middleton Island (Alaska) between 1996 and 2006 (n = 1629) that bred in the same colony through 2013 (n = 235); and (ii) breeding success of individuals that have completed their life cycle at the colony (n = 56). Birds were raised in nests that were either supplemented with food (Fed) or unsupplemented (Unfed). Fledging success was higher in Fed compared with Unfed nests. After accounting for hatching rank, growth and oceanic conditions at fledging, Fed fledglings had a lower probability of recruiting as breeders in the Middleton colony than Unfed birds. The per-nest contribution of breeders was still significantly higher for Fed nests because of their higher productivity. Lifetime reproductive success of a subset of kittiwakes that thus far had completed their life cycle was not affected by the food supplementation during development. Our results cast light on the carry-over effects of early food conditions on the vital rates of long-lived animals and support food supplementation as an effective conservation strategy for long-lived seabirds.

Feather corticosterone reveals developmental stress in seabirds.

In nest-bound avian offspring, food shortages typically trigger a release of the stress hormone corticosterone (CORT). Recent studies indicate that CORT is passively deposited in the tissue of growing feathers and thus may provide an integrated measure of stress incurred during development in the nest. The current hypothesis predicts that, assuming a constant rate of feather growth, elevated CORT circulating in the blood corresponds to higher levels of CORT in feather tissue, but experimental evidence for nutritionally stressed chicks is lacking. Here, we examined how food limitation affects feather CORT content in the rhinoceros auklet (Cerorhinca moncerata). We (i) used captive chicks reared on control versus restricted diets, and (ii) applied this technique to free-living chicks with unknown nutritional histories that fledged at three separate colonies. We found that (i) feather growth was not affected by experimentally induced nutritional stress; (ii) captive chicks raised on a restricted diet had higher levels of CORT in their primary feathers; (iii) feather CORT deposition is a sensitive method of detecting nutritional stress; and (iv) free-living fledglings from the colony with poor reproductive performance had higher CORT in their primary feathers. We conclude that feather CORT is a sensitive integrated measure revealing the temporal dynamics of food limitations experienced by rhinoceros auklet nestlings. The use of feather CORT may be a powerful endocrine tool in ecological and evolutionary studies of bird species with similar preferential allocation of limited resources to feather development.

Migration and stress during reproduction govern telomere dynamics in a seabird.

Changes in telomere length are believed to reflect changes in physiological state and life expectancy in animals. However, much remains unknown about the determinants of telomere dynamics in wild populations, and specifically the influence of conditions during highly mobile life-history stages, for example migration. We tested whether telomere dynamics were associated with migratory behaviour and/or with stress during reproduction in free-living seabirds. We induced short-term stress during reproduction in chick-rearing, black-legged kittiwakes (Rissa tridactyla), tracked winter migration with geolocators and measured telomere length before and after winter migration. We found that time spent at wintering grounds correlated with reduced telomere loss, while stress during reproduction accelerated telomere shortening. Our results suggest that different life-history stages interact to influence telomere length, and that migratory patterns may be important determinants of variation in an individual's telomere dynamics.

Age, sex, and telomere dynamics in a long-lived seabird with male-biased parental care.

The examination of telomere dynamics is a recent technique in ecology for assessing physiological state and age-related traits from individuals of unknown age. Telomeres shorten with age in most species and are expected to reflect physiological state, reproductive investment, and chronological age. Loss of telomere length is used as an indicator of biological aging, as this detrimental deterioration is associated with lowered survival. Lifespan dimorphism and more rapid senescence in the larger, shorter-lived sex are predicted in species with sexual size dimorphism, however, little is known about the effects of behavioral dimorphism on senescence and life history traits in species with sexual monomorphism. Here we compare telomere dynamics of thick-billed murres (Urialomvia), a species with male-biased parental care, in two ways: 1) cross-sectionally in birds of known-age (0-28 years) from one colony and 2) longitudinally in birds from four colonies. Telomere dynamics are compared using three measures: the telomere restriction fragment (TRF), a lower window of TRF (TOE), and qPCR. All showed age-related shortening of telomeres, but the TRF measure also indicated that adult female murres have shorter telomere length than adult males, consistent with sex-specific patterns of ageing. Adult males had longer telomeres than adult females on all colonies examined, but chick telomere length did not differ by sex. Additionally, inter-annual telomere changes may be related to environmental conditions; birds from a potentially low quality colony lost telomeres, while those at more hospitable colonies maintained telomere length. We conclude that sex-specific patterns of telomere loss exist in the sexually monomorphic thick-billed murre but are likely to occur between fledging and recruitment. Longer telomeres in males may be related to their homogamous sex chromosomes (ZZ) or to selection for longer life in the care-giving sex. Environmental conditions appeared to be the primary drivers of annual changes in adult birds.

Effects of food availability on yolk androgen deposition in the black-legged kittiwake (Rissa tridactyla), a seabird with facultative brood reduction.

In birds with facultative brood reduction, survival of the junior chick is thought to be regulated primarily by food availability. In black-legged kittiwakes (Rissa tridactyla) where parents and chicks are provided with unlimited access to supplemental food during the breeding season, brood reduction still occurs and varies interannually. Survival of the junior chick is therefore affected by factors in addition to the amount of food directly available to them. Maternally deposited yolk androgens affect competitive dynamics within a brood, and may be one of the mechanisms by which mothers mediate brood reduction in response to a suite of environmental and physiological cues. The goal of this study was to determine whether food supplementation during the pre-lay period affected patterns of yolk androgen deposition in free-living kittiwakes in two years (2003 and 2004) that varied in natural food availability. Chick survival was measured concurrently in other nests where eggs were not collected. In both years, supplemental feeding increased female investment in eggs by increasing egg mass. First-laid ("A") eggs were heavier but contained less testosterone and androstenedione than second-laid ("B") eggs across years and treatments. Yolk testosterone was higher in 2003 (the year with higher B chick survival) across treatments. The difference in yolk testosterone levels between eggs within a clutch varied among years and treatments such that it was relatively small when B chick experienced the lowest and the highest survival probabilities, and increased with intermediate B chick survival probabilities. The magnitude of testosterone asymmetry in a clutch may allow females to optimize fitness by either predisposing a brood for reduction or facilitating survival of younger chicks.

Thyroid hormones correlate with basal metabolic rate but not field metabolic rate in a wild bird species.

Thyroid hormones (TH) are known to stimulate in vitro oxygen consumption of tissues in mammals and birds. Hence, in many laboratory studies a positive relationship between TH concentrations and basal metabolic rate (BMR) has been demonstrated whereas evidence from species in the wild is scarce. Even though basal and field metabolic rates (FMR) are often thought to be intrinsically linked it is still unknown whether a relationship between TH and FMR exists. Here we determine the relationship between the primary thyroid hormone triiodothyronine (T3) with both BMR and FMR in a wild bird species, the black-legged kittiwake (Rissa tridactyla). As predicted we found a strong and positive relationship between plasma concentrations of T3 and both BMR and mass-independent BMR with coefficients of determination ranging from 0.36 to 0.60. In contrast there was no association of T3 levels with either whole-body or mass-independent FMR (R(2) =0.06 and 0.02, respectively). In accordance with in vitro studies our data suggests that TH play an important role in modulating BMR and may serve as a proxy for basal metabolism in wild birds. However, the lack of a relationship between TH and FMR indicates that levels of physical activity in kittiwakes are largely independent of TH concentrations and support recent studies that cast doubt on a direct linkage between BMR and FMR.

Isotopic segregation between sympatric seabird species increases with nutritional stress.

Dietary segregation is essential for the coexistence of closely related species of animals. However, little is known about how changes in availability of food resources might affect trophic interactions of wild animals breeding in sympatry. Here, we examined how interannual variations in relative food availability (as reflected in blood levels of stress hormone corticosterone, CORT) affect food partitioning (assessed via a comparison of stable isotope δ(15)N and δ(13)C ratios of blood) between the common murre (Uria aalge) and thick-billed murre (Uria lomvia), breeding on a single colony in the Bering Sea. During a 6-year study, CORT varied among years but not between species, whereas stable isotope ratios varied among years and between species. Isotopic distance between species increased with increasing CORT. These results indicate that, when food was not limiting, both species relied on similar food resources. As foraging conditions deteriorated, murres diverged in their diets. We conclude that the degree of dietary segregation between Uria spp. varies with changes in the availability of food and is greatest during food shortages.

Adverse foraging conditions may impact body mass and survival of a high Arctic seabird.

Tradeoffs between current reproduction and future survival are widely recognized, but may only occur when food is limited: when foraging conditions are favorable, parents may be able to reproduce without compromising their own survival. We investigated these tradeoffs in the little auk (Alle alle), a small seabird with a single-egg clutch. During 2005-2007, we examined the relationship between body mass and survival of birds breeding under contrasting foraging conditions at two Arctic colonies. We used corticosterone levels of breeding adults as a physiological indicator of the foraging conditions they encountered during each reproductive season. We found that when foraging conditions were relatively poor (as reflected in elevated levels of corticosterone), parents ended the reproductive season with low body mass and suffered increased post-breeding mortality. A positive relationship between body mass and post-breeding survival was found in one study year; light birds incurred higher survival costs than heavy birds. The results of this study suggest that reproducing under poor foraging conditions may affect the post-breeding survival of long-lived little auks. They also have important demographic implications because even a small change in adult survival may have a large effect on populations of long-lived species.

Changes in glucocorticoids, IGF-I and thyroid hormones as indicators of nutritional stress and subsequent refeeding in Steller sea lions (Eumetopias jubatus).

Physiological responses to changes in energy balance are tightly regulated by the endocrine system through glucocorticoids, IGF-I and thyroid hormones. Changes in these hormones were studied in eight captive female Steller sea lions that experienced changes in food intake, body mass, body composition, and blood metabolites during summer and winter. During a period of energy restriction, one group of sea lions was fed reduced amounts of Pacific herring and another was fed an isocaloric diet of walleye pollock, after which both groups returned to their pre-experimental diets of herring. Cortisol was negatively and IGF-I was positively associated with changes in body mass during periods of energy restriction (mass loss associated with increase in cortisol and decrease in IGF-I) and refeeding (body mass maintenance associated with stable hormone concentrations in summer and compensatory growth linked to decrease in cortisol and increase in IGF-I in winter). Cortisol and IGF-I were also correlated with changes in lipid and lean mass, respectively. Consequently, these two hormones likely make adequate biomarkers for nutritional stress in sea lions, and when combined provide indication of the energetic strategy (lipid vs lean mass catabolism) animals adopt to cope with changes in nutrient intake. Unlike type of diet fed to the sea lions, age of the animals also impacted hormonal responses, with younger animals showing more intense hormonal changes to nutritional stress. Thyroid hormones, however, were not linked to any physiological changes observed in this study.

Size of ornament is negatively correlated with baseline corticosterone in males of a socially monogamous colonial seabird.

The Goymann-Wingfield model predicts that glucocorticoid levels in social animals reflect the costs of acquiring and maintaining social status. The crested auklet is one of the few avian colonial species where a mutual ornament in males and females is used in both sexual and aggressive displays. Previous studies of the crested auklet support the notion that the crest ornament is a badge of status in this species. Here, we examined the relationship between the crest ornament size and the adrenocortical function in breeding crested auklets. Crest length was negatively correlated with corticosterone at baseline in males, but not in females. Baseline corticosterone in females (but not in males) was negatively correlated with body condition index. Although male and female crested auklets are monomorphic in their ornamental traits, our results suggest that the socially mediated physiological costs associated with status signaling may differ between the sexes.

Corticosterone levels of tufted puffins vary with breeding stage, body condition index, and reproductive performance.

Corticosterone (CORT) levels in free-living animals are seasonally modulated and vary with environmental conditions. Although most studies measure total CORT concentrations, levels of corticosteroid binding globulin (CBG) may also be modulated, thus altering the concentration of CORT available for diffusion into tissues (free CORT). We investigated the seasonal dynamics of CBG, total CORT, and free CORT in breeding tufted puffins (Fratercula cirrhata) during 2 years characterized by high rates of nestling growth and survival. We then compared concentrations of total CORT in this population to levels in chick-rearing puffins at another colony during 2 years with low productivity. At the high productivity colony, levels of CBG, total baseline CORT, free baseline CORT, and total maximum CORT were all higher prior to egg-laying than during late incubation and late chick-rearing. Levels of CBG were positively correlated with body condition index (BCI) and free baseline CORT was negatively correlated with BCI. Total baseline levels of CORT during chick-rearing were two to four times higher at the colony with low rates of nestling growth and survival. Our results demonstrate the need for long-term datasets to disentangle seasonal trends in CORT levels from trends driven by changes in environmental conditions. Given the negative effects associated with chronic elevation of CORT, our results indicate the cost of reproduction may be higher during years characterized by low productivity.