Compensatory Growth Potential Research Articles

Dynamic subcanopy leaf traits drive resistance of net primary production across a disturbance severity gradient

Across the globe, the forest carbon sink is increasingly vulnerable to an expanding array of low- to moderate-severity disturbances. However, some forest ecosystems exhibit functional resistance (i.e., the capacity of ecosystems to continue functioning as usual) following disturbances such as extreme weather events and insect or fungal pathogen outbreaks. Unlike severe disturbances (e.g., stand-replacing wildfires), moderate severity disturbances do not always result in near-term declines in forest production because of the potential for compensatory growth, including enhanced subcanopy production. Community-wide shifts in subcanopy plant functional traits, prompted by disturbance-driven environmental change, may play a key mechanistic role in resisting declines in net primary production (NPP) up to thresholds of canopy loss. However, the temporal dynamics of these shifts, as well as the upper limits of disturbance for which subcanopy production can compensate, remain poorly characterized. In this study, we leverage a 4-year dataset from an experimental forest disturbance in northern Michigan to assess subcanopy community trait shifts as well as their utility in predicting ecosystem NPP resistance across a wide range of implemented disturbance severities. Through mechanical girdling of stems, we achieved a gradient of severity from 0% (i.e., control) to 45, 65, and 85% targeted gross canopy defoliation, replicated across four landscape ecosystems broadly representative of the Upper Great Lakes ecoregion. We found that three of four examined subcanopy community weighted mean (CWM) traits including leaf photosynthetic rate (p = 0.04), stomatal conductance (p = 0.07), and the red edge normalized difference vegetation index (p < 0.0001) shifted rapidly following disturbance but before widespread changes in subcanopy light environment triggered by canopy tree mortality. Surprisingly, stimulated subcanopy production fully compensated for upper canopy losses across our gradient of experimental severities, achieving complete resistance (i.e., no significant interannual differences from control) of whole ecosystem NPP even in the 85% disturbance treatment. Additionally, we identified a probable mechanistic switch from nutrient-driven to light-driven trait shifts as disturbance progressed. Our findings suggest that remotely sensed traits such as the red edge normalized difference vegetation index (reNDVI) could be particularly sensitive and robust predictors of production response to disturbance, even across compositionally diverse forests. The potential of leaf spectral indices to predict post-disturbance functional resistance is promising given the capabilities of airborne to satellite remote sensing. We conclude that dynamic functional trait shifts following disturbance can be used to predict production response across a wide range of disturbance severities.

Comparative analysis of different density restrictions reveals the potential influence mechanism on the compensatory growth of Litopenaeus vannamei

Shrimp nursery rearing technology is increasingly being used by aquatic farmers and enterprises. Determining an appropriate density restriction in order to obtain a greater compensatory growth potential is the key to this technology. Based on the industry standards for indoor shrimp farming, three densities for Litopanaeus vannamei nursery rearing were examined (D1 [control] = 10,000 PL/m3, D3 = 30,000 PL/m3, and D5 = 50,000 PL/m3). The results showed that the D5 group had an over-compensation growth effect, whereas the D3 group showed a full-compensation growth effect. A preliminary investigation of the mechanism of compensatory growth was explored. The results showed that during the compensation stage, the SGR (Special Growth Rate) and FCE (Feed Conversion Efficiency) of the D5 group were significantly higher (p < 0.05) than the control. T-SOD enzyme activity was not significantly different (p > 0.05) from the control. Antioxidants such as CAT, GSH-PX and MDA all had compensatory changes. In addition, the relative mRNA expression of several genes was measured. The results showed that growth-related genes (EGFR, MSTN), molting-related genes (MIH), immune-related genes (Toll) and digestion-related genes (α-amylase) had a relative compensation of mRNA expression. Meanwhile, transcriptome analysis of shrimps after different density restrictions in the compensation stage was performed. Totally 237 and 348 differentially expression genes (DEGs) were identified in the D5- and D3-treated shrimps, respectively. In D5-treated shrimps, DEGs were annotated and grouped into nine processes or pathways related to animal metabolic response. With respect to D3-treated shrimps, DEGs were mainly annotated to 15 processes or pathways related to animal metabolic response. Therefore, this study provides a basis for the theory and practice of compensatory growth during the nursery rearing of commercial shrimp.

Proactive coping style in early emerging rainbow trout carries a metabolic cost with no apparent return

The timing with which salmonid larvae emerge from their gravel nests is thought to be correlated with a particular suite of behavioural and physiological traits that correspond to the stress coping style of the individual. Among these traits, aggressiveness, dominance and resilience to stress, are potentially interesting to exploit in aquaculture production. In the present study a series of experiments were performed, with the purpose of characterising behavioural, metabolic and production related traits in rainbow trout juveniles from different emergence fractions. Newly hatched rainbow trout were sorted according to their emergence time from an artificial redd. The early, middle, and late fractions were retained and assessed for their physiological response to stress, growth performance, metabolism, fasting tolerance, and potential for compensatory growth. The early emerging fraction showed proactive behavioural traits; they were faster to reappear following startling, showed a reduced cortisol response following stress, and a reduced metabolic cost of recovery. Emergence time was not correlated with any differences in standard or maximum metabolic rates, but was however, correlated with higher routine metabolic rates, as demonstrated by significantly bigger weight losses during fasting in the early emerging group. Growth rates and feed conversion efficiencies were not significantly different when fish were co-habitated under a restrictive feeding regime, suggesting that early emerging fish are not able to monopolise food resources. The intermediate emerging group, which makes up the bulk of a population and is often ignored, appears to possess the best growth performance traits, possibly because they do not expend excessive energy on dominance behaviour such as the early emerging group, while they are also not overly timid or stress prone such as the late emerging group.

Plane of nutrition affects the phylogenetic diversity and relative abundance of transcriptionally active methanogens in the bovine rumen

Methane generated during enteric fermentation in ruminant livestock species is a major contributor to global anthropogenic greenhouse gas emissions. A period of moderate feed restriction followed by ad libitum access to feed is widely applied in cattle management to exploit the animal’s compensatory growth potential and reduce feed costs. In the present study, we utilised microbial RNA from rumen digesta samples to assess the phylogenetic diversity of transcriptionally active methanogens from feed-restricted and non-restricted animals. To determine the contribution of different rumen methanogens to methanogenesis during dietary restriction of cattle, we conducted high-throughput mcrA cDNA amplicon sequencing on an Illumina MiSeq and analysed both the abundance and phylogenetic origin of different mcrA cDNA sequences. When compared to their unrestricted contemporaries, in feed-restricted animals, the methanogenic activity, based on mcrA transcript abundance, of Methanobrevibacter gottschalkii clade increased while the methanogenic activity of the Methanobrevibacter ruminantium clade and members of the Methanomassiliicoccaceae family decreased. This study shows that the quantity of feed consumed can evoke large effects on the composition of methanogenically active species in the rumen of cattle. These data potentially have major implications for targeted CH4 mitigation approaches such as anti-methanogen vaccines and/or tailored dietary management.

Effect of anticoccidial monensin with oregano essential oil on broilers experimentally challenged with mixed Eimeria spp

Essential oil of oregano ( OEO: ) has proven to be a potential candidate for controlling chicken coccidiosis. The aim of the current study is to determine whether OEO and an approved anticoccidial, monensin sodium ( MON: ), as in-feed supplements could create a synergism when combined at low dosages. Day-old broiler chickens were separated into six equal groups with six replicate pens of 36 birds. One of the groups was given a basal diet and served as the control ( CNT: ). The remaining groups received the basal diet supplemented with 100 mg/kg MON, 50mg/kg MON, 24 mg/kg OEO, 12 mg/kg OEO, or 50mg/kg MON + 12 mg/kg OEO. All of the chickens were challenged with field-type mixed Eimeria species at 12 d of age. Following the infection (i.e., d 13 to 42), the greatest growth gains and lowest feed conversion ratio values were recorded for the group of birds fed 100 mg/kg MON (P < 0.05), whereas results for the CNT treatment were inferior. Dietary OEO supplementations could not support growth to a level comparable with the MON (100 mg/kg). The MON programs were more efficacious in reducing fecal oocyst numbers compared to CNT and OEO treatments (P < 0.05). Serum malondialdehyde and nitric oxide concentrations were decreased (P < 0.01), whereas superoxide dismutase (P < 0.05) and total antioxidant status (P < 0.01) were increased in response to dietary medication with MON and OEO. All MON and OEO treatments conferred intestinal health benefits to chickens by improving their morphological development and enzymatic activities. The results suggest that OEO supported the intestinal absorptive capacity and antioxidant defense system during Eimeria infection; however, it displayed little direct activity on the reproductive capacity of Eimeria This might be the reason for inferior compensatory growth potential of OEO compared to that MON following the challenge. Combination MON with OEO was not considered to show promise for controlling chicken coccidiosis because of the lack of a synergistic or additive effect.

Population divergence in compensatory growth responses and their costs in sticklebacks.

Compensatory growth (CG) may be an adaptive mechanism that helps to restore an organisms’ growth trajectory and adult size from deviations caused by early life resource limitation. Yet, few studies have investigated the genetic basis of CG potential and existence of genetically based population differentiation in CG potential. We studied population differentiation, genetic basis, and costs of CG potential in nine-spined sticklebacks (Pungitius pungitius) differing in their normal growth patterns. As selection favors large body size in pond and small body size in marine populations, we expected CG to occur in the pond but not in the marine population. By manipulating feeding conditions (viz. high, low and recovery feeding treatments), we found clear evidence for CG in the pond but not in the marine population, as well as evidence for catch-up growth (i.e., size compensation without growth acceleration) in both populations. In the marine population, overcompensation occurred individuals from the recovery treatment grew eventually larger than those from the high feeding treatment. In both populations, the recovery feeding treatment reduced maturation probability. The recovery feeding treatment also reduced survival probability in the marine but not in the pond population. Analysis of interpopulation hybrids further suggested that both genetic and maternal effects contributed to the population differences in CG. Hence, apart from demonstrating intrinsic costs for recovery growth, both genetic and maternal effects were identified to be important modulators of CG responses. The results provide an evidence for adaptive differentiation in recovery growth potential.

Tolerance of an expanding subarctic shrub, Betula glandulosa, to simulated caribou browsing.

Densification of the shrub layer has been reported in many subarctic regions, raising questions about the implication for large herbivores and their resources. Shrubs can tolerate browsing and their level of tolerance could be affected by browsing and soils productivity, eventually modifying resource availability for the caribou. Our objective was to assess the compensatory growth potential of a subarctic shrub, Betula glandulosa Michx., in relation with caribou browsing and nutriment availability for the plants. We used a simulated browsing (0, 25 and 75% of available shoots) and nitrogen-fertilisation (0 and 10 g m−2) experiment to test two main hypotheses linking tolerance to resource availability, the Compensatory Continuum Hypothesis and the Growth Rate Hypothesis as well as the predictions from the Limiting Resource Model. We seek to explicitly integrate the relative browsing pressure in our predictions since the amount of tissues removed could affect the capacity of long-lived plants to compensate. Birches fully compensated for moderate browsing with an overall leaf biomass similar to unbrowsed birches but undercompensated under heavy browsing pressure. The main mechanism explaining compensation appears to be the conversion of short shoots into long shoots. The leaf area increased under heavy browsing pressure but only led to undercompensation. Fertilisation for two consecutive years did not influence the response of birch, thus we conclude that our results support the LRM hypothesis of equal tolerance under both high and low nitrogen availability. Our results highlight that the potential for compensatory growth in dwarf birch is surpassed under heavy browsing pressure independently of the fertilisation regime. In the context of the worldwide decline in caribou herds, the reduction in browsing pressure could act synergistically with global climate change to promote the current shrub expansion reported in subarctic regions.

Quantification and Three-Dimensional Imaging of the Insulitis-Induced Destruction of β-Cells in Murine Type 1 Diabetes

OBJECTIVEThe aim of this study was to refine the information regarding the quantitative and spatial dynamics of infiltrating lymphocytes and remaining β-cell volume during the progression of type 1 diabetes in the nonobese diabetic (NOD) mouse model of the disease.RESEARCH DESIGN AND METHODSUsing an ex vivo technique, optical projection tomography (OPT), we quantified and assessed the three-dimensional spatial development and progression of insulitis and β-cell destruction in pancreata from diabetes-prone NOD and non–diabetes-prone congenic NOD.H-2b mice between 3 and 16 weeks of age.RESULTSTogether with results showing the spatial dynamics of the insulitis process, we provide data of β-cell volume distributions down to the level of the individual islets and throughout the pancreas during the development and progression of type 1 diabetes. Our data provide evidence for a compensatory growth potential of the larger insulin+ islets during the later stages of the disease around the time point for development of clinical diabetes. This is in contrast to smaller islets, which appear less resistant to the autoimmune attack. We also provide new information on the spatial dynamics of the insulitis process itself, including its apparently random distribution at onset, the local variations during its further development, and the formation of structures resembling tertiary lymphoid organs at later phases of insulitis progression.CONCLUSIONSOur data provide a powerful tool for phenotypic analysis of genetic and environmental effects on type 1 diabetes etiology as well as for evaluating the potential effect of therapeutic regimes.

Variation in grazing tolerance among three tallgrass prairie plant species

Three tallgrass prairie plant species, two common perennial forbs (Artemisia ludoviciana and Aster ericoides [Asteraceae]) and a dominant C(4) perennial grass (Sorghastrum nutans) were studied under field and greenhouse conditions to evaluate interspecific variation in grazing tolerance (compensatory growth capacity). Adaptation to ungulate grazing was also assessed by comparing defoliation responses of plants from populations with a 25-yr history of no grazing or moderate ungulate grazing. Under field conditions, all three species showed significant reductions in shoot relative growth rates (RGR), biomass, and reproduction with defoliation. In the two forbs, clipping resulted in negative shoot RGR and reductions in both number and length of shoot branches per ramet. Sorghastrum nutans maintained positive RGR under defoliation due to a compensatory increase in leaf production. Defoliation reduced rhizome production in A. ericoides and S. nutans, but not in A. ludoviciana. Clipping significantly reduced sexual reproductive allocation in all three species, although S. nutans showed a smaller reduction than the forbs. All three species showed similar responses to defoliation in burned and unburned sites. Under greenhouse conditions, a similar clipping regimen resulted in smaller reductions in growth and reproduction than those observed in the field. For all three species, the grazing tolerance indices calculated under natural field conditions were significantly lower than those estimated from greenhouse-grown plants, and the interspecific patterns of grazing tolerance were different. Aster ericoides exhibited the highest overall defoliation tolerance under greenhouse conditions, followed by S. nutans. Artemisia ludoviciana, the only study species that is typically not grazed by ungulates in the field, showed the lowest grazing tolerance. In the field experiment S. nutans showed the highest grazing tolerance and the two forbs had similar low tolerance indices. These patterns indicate that, despite high compensatory growth potential, limited resource availability and competition in the field significantly reduce the degree of compensation and alter interspecific differences in grazing tolerance among prairie plants. In all three species, defoliation suppressed sexual reproduction more than growth or vegetative reproduction. Significant interactions between plant responses to defoliation and site of origin (historically grazed or ungrazed sites) for some response variables (root/shoot ratios, rhizome bud initiation, and reproductive allocation) indicated some degree of population differentiation and genetic adaptation in response to a relatively short history of ungulate grazing pressure. The results of this study indicate that patterns of grazing tolerance in tallgrass prairie are both genetically based and also environmentally dependent.

Do Species Mixtures Increase Above‐ and Belowground Resource Capture in Woody and Herbaceous Tropical Legumes?

The rotation of crops with planted, N2‐fixing legumes is a promising agroforestry innovation for replenishing soil fertility in the tropics. We postulated that woody and herbaceous legumes with different growth and rooting patterns could be mixed to optimize above‐ and belowground resource capture. The objective of this study was to evaluate the effect of species interactions on resource utilization by legumes grown in mixtures on a Kandiudalfic Eutrudox in western Kenya. Four woody legume shrubs—pigeonpea [Cajanus cajan (L.) Millsp.], sesbania [Sesbania sesban (L.) Merr.], crotalaria (Crotalaria grahamiana Wight and Arn.), and tephrosia (Tephrosia vogelii Hook F.)—grown in monoculture and mixed stands were evaluated for light interception, soil N and water uptake, and biomass production. Siratro [Macroptilium atropurpureum (DC.) Urb.] and groundnut (Arachis hypogaea L.) were undersown in woody legume stands. Total aboveground biomass production ranged from 9 to 13 Mg ha−1 for monoculture and 8 to 15 Mg ha−1 for mixtures of woody legumes. Total N in woody‐legume stands ranged from 100 to 178 kg N ha−1. Biomass and plant N were not significantly different among woody‐legume treatments. However, undersowing siratro as a supplement increased stand productivity and recycled biomass N. Species complementarity in topsoil and subsoil utilization of mineral N was observed in crotalaria + sesbania and pigeonpea + tephrosia mixed stands. Dense soil cover created by siratro led to better conservation of soil water. Results indicated that the tested mixtures provide a better risk management strategy through compensatory growth potential. Greatest opportunities for intensifying resource utilization appear to exist through undersowing a creeping legume with an open‐canopy woody legume.

Do Species Mixtures Increase Above- and Belowground Resource Capture in Woody and Herbaceous Tropical Legumes?

The rotation of crops with planted, N2-fixing legumes is a promising agroforestry innovation for replenishing soil fertility in the tropics. We postulated that woody and herbaceous legumes with different growth and rooting patterns could be mixed to optimize above- and belowground resource capture. The objective of this study was to evaluate the effect of species interactions on resource utilization by legumes grown in mixtures on a Kandiudalfic Eutrudox in western Kenya. Four woody legume shrubs—pigeonpea [Cajanus cajan (L.) Millsp.], sesbania [Sesbania sesban (L.) Merr.], crotalaria (Crotalaria grahamiana Wight and Arn.), and tephrosia (Tephrosia vogelii Hook F.)—grown in monoculture and mixed stands were evaluated for light interception, soil N and water uptake, and biomass production. Siratro [Macroptilium atropurpureum (DC.) Urb.] and groundnut (Arachis hypogaea L.) were undersown in woody legume stands. Total aboveground biomass production ranged from 9 to 13 Mg ha−1 for monoculture and 8 to 15 Mg ha−1 for mixtures of woody legumes. Total N in woody-legume stands ranged from 100 to 178 kg N ha−1. Biomass and plant N were not significantly different among woody-legume treatments. However, undersowing siratro as a supplement increased stand productivity and recycled biomass N. Species complementarity in topsoil and subsoil utilization of mineral N was observed in crotalaria + sesbania and pigeonpea + tephrosia mixed stands. Dense soil cover created by siratro led to better conservation of soil water. Results indicated that the tested mixtures provide a better risk management strategy through compensatory growth potential. Greatest opportunities for intensifying resource utilization appear to exist through undersowing a creeping legume with an open-canopy woody legume.

Patchiness and compensatory growth in a fungus-Collembola system.

The compensatory growth potential of a grazed fungal biomass was mathematically expressed as a function of patchiness in its distribution and demonstrated in an experiment using the fungivorous collembolan Onychiurus armatus and the soil fungi Verticillium bulbillosum and Penicillium spinulosum. The model addresses the regrowth potential in relation to patch fragmentation, travelling time and consumption rate of the collembolan and the mean relative growth rate of the fungus. It suggests that the mean relative growth rate required for regrowth decreases with patch fragmentation and increases with the mean growth rate of the fungus. The experiments were performed with a system of soil-filled vials provided with fungi and collembolans. The size of the vials and the length of the tubes connecting them were varied to give different patch sizes and travelling times. The respiratory activity of fungi after grazing increased as a unit of mycelium was distributed into smaller connected vials. The slow growing species V. bulbillosum showed a greater but delayed response to grazing in comparison with the fast growing P. spinulosum. An increased travelling time delayed the growth response in both species.

Impact of SO 2 Exposure on the Response of Agropyron smithii to Defoliation

Agropyron smithii populations exposed to 3 controlled SO2 concentrations were defoliated either once or twice during the growing season at a light and a heavy intensity. The intensity and frequency of defoliation were most influential in determining growth and tillering responses. Defoliating twice, at either intensity, had a large negative impact on plant growth whereas compensatory growth occurred after defoliating once at either intensity. Sulfur dioxide alone had no significant effect on biomass or the number of tillers, even though sulfur accumulated approximately in proportion to exposure concentration. Sulfur dioxide exposure with the additional influence of defoliation affected both the regrowth of A. smithii in terms of biomass and tiller numbers and forage sulfur concentration. Decreased plant growth in response to SO2 plus defoliation was dependent on defoliation frequency, whereas the effect of SO2 plus defoliation on plant sulfur concentration was positive and negative and depended on a complex interaction of SO2 concentration and defoliation frequency and intensity. The results are discussed in relation to the shortand long-term compensatory growth potential of a system simultaneously exposed to grazing and air pollution and the potential effect on consumers. During the first 4 years of a field experiment designed to investigate the response of a native North American grassland to controlled low concentrations of sulfur dioxide, it was observed that exposures during the growing season had subtle, but potentially important effects upon the system (Lauenroth and Heasley 1980). For example, exposure of Agropyron smithii Rydb. to S02 reduced chlorophyll concentration (Lauenroth and Dodd 1981), increased sulfur concentration (Lauenroth et al. 1979, Milchunas et al. 198 la), decreased the functional lives of leaves (Heitschmidt et al. 1978, Milchunas et al. 198 lb), and decreased the amount of labile carbon stored in the rhizomes (Lauenroth and Heasley 1980). Regrowth of A. smithii in the spring or after defoliation is thought to be dependent upon carbohydrates stored in rhizomes and roots (Bokhari 1977). Before the SO2 treatments were begun the area had been grazed by cattle. Following exclusion of cattle, a significant year to year increment in rhizome biomass was observed on the control plot. This was interpreted as an indication of recovery from grazing. B3y contrast, rhizome biomass failed to recover on the 170 ,Ag . mSO2 treatment. This suggested that, although the mechanisms by which SO2 exposure and grazing effect plants are different, the response of the plants to SO2 or grazing may be similar and/or additive. Populations under stress are often considered to be more susceptible to damage caused by additional perturbations. Because of the importance of these grasslands to the livestock economy of the northern Great Plains and the high probability that coal combustion for electric power production will increase in this area, a field experiment was conducted to examine the potential interactions between defoliation and SO2 exposure on the native vegetation. The hypothesis was that defoliation would be more detrimental to Authors are associate professor, Range Science Department, and Natural Resource Ecology Laboratory; associate director, Natural Resource Ecology Laboratory, and associate professor, Range Science Department; research associate, Natural Resource Ecology Laboratory, Colorado State University, Fort Collins; and professor, Range Management Division, University of Wyoming, Laramie. Manuscript accepted April 30, 1984. regrowth of A. smithii populations which had been exposed to S02 for 4 years than to populations not exposed to SO2.

Carbon/Nutrient Balance of Boreal Plants in Relation to Vertebrate Herbivory

The evolutionary response of plants to herbivory is constrained by the availability of resources in the environment. Woody plants adapted to low-resource environments have intrinsically slow growth rates that limit their capacity to grow rapidly beyond the reach of most browsing mammals. Their low capacity to acquire resources limits their potential for compensatory growth which would otherwise enable them to replace tissue destroyed by browsing. Plants adapted to low-resource environments have responded to browsing by evolving strong constitutive defenses with relatively low ontogenetic plasticity. Because nutrients are often more limiting than light in boreal forests, slowly growing boreal forest trees utilize carbon-based rather than nitrogen-based defenses. More rapidly growing shade-intolerant trees that are adapted to growth in high-resource environments are selected for competitive ability and can grow rapidly beyond the range of most browsing mammals. Moreover, these plants have the carbon and nutrient reserves necessary to replace tissue lost to browsing through compensatory growth. However, because browsing of juvenile plants reduces vertical growth and thus competitive ability, these plants are selected for resistance to browsing during the juvenile growth phase. Consequently, early successional boreal forest trees have responded to browsing by evolving strong defenses during juvenility only. Because severe pruning causes woody plants to revert to a juvenile form, resistance of woody plants to hares increases after severe hare browsing as occurs during hare population outbreaks. This increase in browsing resistance may play a significant role in boreal forest plant-hare interactions. Unlike woody plants, graminoids retain large reserves of carbon and nutrients below ground in both low-resource and high-resource environments and can respond to severe grazing through compensatory growth. These fundamental differences between the response of woody plants and graminoids to vertebrate herbivory suggest that the dynamics of browsing systems and grazing systems are qualitatively different.