Large old trees increase growth under shifting climatic constraints: Aligning tree longevity and individual growth dynamics in primary mountain spruce forests

In a world of accelerating changes in environmental conditions driving tree growth, tradeoffs between tree growth rate and longevity could curtail the abundance of large old trees (LOTs), with potentially dire consequences for biodiversity and carbon storage. However, the influence of tree-level tradeoffs on forest structure at landscape scales will also depend on disturbances, which shape tree size and age distribution, and on whether LOTs can benefit from improved growing conditions due to climate warming. We analyzed temporal and spatial variation in radial growth patterns from ~5000 Norway spruce (Picea abies [L.] H. Karst) live and dead trees from the Western Carpathian primary spruce forest stands. We applied mixed-linear modeling to quantify the importance of LOT growth histories and stand dynamics (i.e., competition and disturbance factors) on lifespan. Finally, we assessed regional synchronization in radial growth variability over the 20th century, and modeled the effects of stand dynamics and climate on LOTs recent growth trends. Tree age varied considerably among forest stands, implying an important role of disturbance as an age constraint. Slow juvenile growth and longer period of suppressed growth prolonged tree lifespan, while increasing disturbance severity and shorter time since last disturbance decreased it. The highest age was not achieved only by trees with continuous slow growth, but those with slow juvenile growth followed by subsequent growth releases. Growth trend analysis demonstrated an increase in absolute growth rates in response to climate warming, with late summer temperatures driving the recent growth trend. Contrary to our expectation that LOTs would eventually exhibit declining growth rates, the oldest LOTs (>400 years) continuously increase growth throughout their lives, indicating a high phenotypic plasticity of LOTs for increasing biomass, and a strong carbon sink role of primary spruce forests under rising temperatures, intensifying droughts, and increasing bark beetle outbreaks.     

A potential tradeoff between feeding rate and aversive learning determines intoxication in a Caenorhabditis elegans host-pathogen system

Despite being the first line of defense against infection, little is known about how host-pathogen interactions determine avoidance. Caenorhabditis elegans can become infected by chemoattractant-producing bacteria through ingestion. The worms can learn to associate these chemoattractants with harm through aversive learning. As a result, the worms will avoid the pathogen. Evolutionary constraints have likely shaped the attraction, intoxication and learning dynamics between bacteria and C. elegans, but these have not been explored. Using bacteria engineered to express an acylhomoserine lactone chemoattractant and a nematicidal protein, we explored how manipulating the amount of attractant produced by the bacteria affects learning and intoxication in mixed stage populations of C. elegans. We found that increasing the production rate of the chemoattractant increased the feeding rate in C. elegans, but decreased the time required for C. elegans to learn to avoid the chemoattractant. Learning generally coincided with a decreased feeding rate. We also observed that the percentage of intoxicated worms was maximized at intermediate production rates of the attractant. We propose that interactions between attractant driven feeding rate and aversive learning are likely responsible for this trend. Our results increase our understanding of behavioral avoidance in C. elegans and have implications in understanding host-pathogen dynamics that shape avoidance.     

Water availability and population origin affect the expression of the tradeoff between reproduction and growth in Plantago coronopus

Investment in reproduction and growth represent a classic tradeoff with implication for life history evolution. The local environment can play a major role in the magnitude and evolutionary consequences of such a tradeoff. Here, we examined the investment in reproductive and vegetative tissue in 40 maternal half‐sib families from four different populations of the herb Plantago coronopus growing in either a dry or wet greenhouse environment. Plants originated from populations with an annual or a perennial life form, with annuals prevailing in drier habitats with greater seasonal variation in both temperature and precipitation. We found that water availability affected the expression of the tradeoff (both phenotypic and genetic) between reproduction and growth, being most accentuated under dry condition. However, populations responded very differently to water treatments. Plants from annual populations showed a similar response to drought condition with little variation among maternal families, suggesting a history of selection favouring genotypes with high allocation to reproduction when water availability is low. Plants from annual populations also expressed the highest level of plasticity. For the perennial populations, one showed a large variation among maternal families in resource allocation and expressed significant negative genetic correlations between reproductive and vegetative biomass under drought. The other perennial population showed less variation in response to treatment and had trait values similar to those of the annuals, although it was significantly less plastic. We stress the importance of considering intraspecific variation in response to environmental change such as drought, as conspecific plants exhibited very different abilities and strategies to respond to high versus low water availability even among geographically close populations.     

Plant chemical defence allocation constrains evolution of local range

Many species of plants in the wild are distributed spatially in patches, the boundaries of which may occur and change because of a complicated interplay between myriad environmental stressors and limitations of, or constraints on, plant coping mechanisms. By examining genetic variation and co‐variation among marker‐inferred inbred lines and sib‐families of an upland wild mustard species within and just a few meters across a natural patch boundary, we show that the evolution of tolerance to the stressful environment outside the patch may be constrained by allocation to glucosinolate compounds (GS) that are defensive against generalist insect herbivores. Several potential stressors were associated with the patch boundary, but carbon isotope ratios indicated that sib‐families with smaller stomatal apertures maintained performance better in response to late season dry conditions, suggesting that drought was an important stressor. The presence of GS may help explain the characteristic patchy distribution of mustards, a relatively diverse and important plant family. This result challenges one end of the continuum of the long‐standing Plant Apparency hypothesis, which essentially states the opposite causation, that low molecular weight toxins like GS are evolutionary responses of patchy distributions and correlated life‐history traits.     

High temperature slows down growth in tobacco hornworms (Manduca sexta larvae) under food restriction

When fed ad libitum (AL), ectothermic animals usually grow faster and have higher metabolic rate at higher ambient temperature. However, if food supply is limited, there is an energy tradeoff between growth and metabolism. Here we hypothesize that for ectothermic animals under food restriction (FR), high temperature will lead to a high metabolic rate, but growth will slow down to compensate for the high metabolism. We measure the rates of growth and metabolism of 4 cohorts of 5th instar hornworms (Manduca sexta larvae) reared at 2 levels of food supply (AL and FR) and 2 temperatures (20 and 30 °C). Our results show that, compared to the cohorts reared at 20 °C, the ones reared at 30 °C have high metabolic rates under both AL and FR conditions, but a high growth rate under AL and a low growth rate under FR, supporting this hypothesis.     

Non-equivalence of growth arrest induced by predation risk or food limitation: context-dependent compensatory growth in anuran tadpoles

1. To gain insight into the evolution of compensatory growth, we studied the growth patterns of anuran (Rana temporaria) larvae following either a period of exogenous growth depression (food restriction) or a period of endogenous depression (exposure to predators). We also investigated the potential deferred costs that larval compensatory growth could impose on post-metamorphic individuals. 2. Food-deprived larvae exhibited full compensatory growth in response to reduced growth rates caused by food limitation, and the growth trajectories of low- and high-rations tadpoles converged before the onset of metamorphosis. 3. According to our predictions, individuals exposed to larval predators did not show growth compensation following predator removal despite undergoing a significant reduction in growth rate associated with low activity levels. 4. Jumping ability of individuals exposed to predators during only 20 days from the commencement of the larval phase was equivalent to that of non-exposed animals, and greater than the jumping capacity of those maintained with predators until the time of metamorphosis. This pattern was consistent with the pattern observed for variation in relative leg length. 5. These results support the suggestion that submaximum and compensatory growth could have evolved to minimize the overall growth/mortality costs in environments with high spatiotemporal variation in predation intensity.     

A high standard metabolic rate constrains juvenile growth

The allocation of energy to various components of an individual's energy budget is often viewed as a competitive process. As such, a tradeoff may exist between production (growth) and maintenance metabolism. One view of a potential tradeoff, termed “the principle of allocation”, suggests that individuals with lower maintenance metabolic expenditures may have higher growth rates. To determine whether such a tradeoff exists, I analyzed the relationship between growth rate and maintenance metabolism of 225 juvenile snapping turtles housed in the laboratory. I measured growth from hatching to 6 months of age, and then measured oxygen consumption and calculated standard metabolic rate. Mean growth rate was 0.19 g d⁻ and mean standard metabolic rate (SMR) was 1.41 kJ d⁻. Maintenance metabolism and growth were negatively correlated after both were adjusted for body mass. The results support the “principle of allocation” theory: individuals with higher standard metabolic rates tended to have low growth rates.     

Linear and threshold-dependent expression of secondary sexual traits in the same individual: insights from a horned beetle (Coleoptera: Scarabaeidae)

Elaborate horns or horn‐like structures in male scarab beetles commonly scale with body size either (a) in a linear fashion with horn size increasing relatively faster than body size or (b) in a threshold‐dependent, sigmoid fashion; that is, males smaller than a certain critical body size develop no or only rudimentary horns, whereas males larger than the threshold size express fully developed horns. The development of linear vs. sigmoid scaling relationships is thought to require fundamentally different regulatory mechanisms. Here we show that such disparate regulatory mechanisms may co‐occur in the same individual. Large males of the south‐east Asian Onthophagus (Proagoderus) watanabei (Ochi & Kon) (Scarabaeidae, Onthophagini) develop a pair of long, curved head horns as well as a single thoracic horn. We show that unlike paired head horns in a large number of Onthophagus species, in O. watanabei the relationship between head horns and body size is best explained by a linear model. Large males develop disproportionately longer horns than small males, but the difference in relative horn sizes across the range of body sizes is small compared to other Onthophagus species. However, the scaling relationship between the thoracic horn and body size is best explained by a strongly sigmoid model. Only males above a certain body size threshold express a thoracic horn and males smaller than this threshold express no horn at all. We found a significant positive correlation between head and thoracic horn length residuals, contrary to what would be expected if a resource allocation tradeoff during larval development would influence the length of both horn types. Our results suggest that the scaling relationship between body size and horn length, and the developmental regulation underlying these scaling relationships, may be quite different for different horns, even though these horns may develop in the same individual. We discuss our results in the context of the developmental biology of secondary sexual traits in beetles. © 2004 The Linnean Society of London, Biological Journal of the Linnean Society, 2004, 83 , 473–480.     

Tradeoff between height and relative growth rate in a dominant grass from the Serengeti ecosystem

We determined the relationship between plant height and whole-plant relative growth rate (g g^-1 day^-1) for ten genotypes of Sporobolus kentrophyllus collected from an intensively grazed site on the Serengeti Plains, Tanzania. Plants were grown for 7 weeks in a greenhouse in Syracuse, N.Y., and harvested weekly. Plants that received simulated bovine urine showed a negative relationship between plant height and growth rate, suggesting a genetic tradeoff between competitive ability if ungrazed (height) and ability to recover from grazing (growth rate). There was no height-growth rate relationship under nitrogen addition rates similar to field mineralization rates. In addition, faster-growing, shorter plants tended to have relatively higher above-ground growth rates than slower-growing, taller plants. These results suggest that natural selection has maintained a gradient of morphologies within this species ranging from short, rapidly growing genotypes adapted to intense grazing conditions to tall, slow-growing, grazer-susceptible genotypes that are superior light competitors in absence of herbivory.