Research Article |
Corresponding author: Bernice Dixie ( b.dixie@uea.ac.uk ) Academic editor: Elisabeth Hornung
© 2015 Bernice Dixie, Hollie White, mark Hassall.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Dixie B, White H, Hassall M (2015) Effects of microclimate on behavioural and life history traits of terrestrial isopods: implications for responses to climate change. In: Taiti S, Hornung E, Štrus J, Bouchon D (Eds) Trends in Terrestrial Isopod Biology. ZooKeys 515: 145–157. https://doi.org/10.3897/zookeys.515.9399
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The sensitivity of terrestrial isopods to changes in both temperature and moisture make them suitable models for examining possible responses of arthropod macro-decomposers to predicted climate change. Effects of changes in both temperature and relative humidity on aggregation, growth and survivorship of species of isopods contrasting in their morphological and physiological adaptations to moisture stress have been investigated in laboratory microcosms.
All three traits were more sensitive to a reduction in relative humidity of 20–25% than they were to an increase in temperature of 5–6 °C. These results suggest that predicted changes in climate in south east England may reduce the extent to which soil animals stimulate microbial activity and hence carbon dioxide (CO2) emissions from soils in the future. This may help to mitigate the potential for a positive feedback between increased CO2 emissions from soils, and increased greenhouse effects causing an increase in soil temperatures.
Temperature, moisture, aggregation, growth rates, mortality rates, stimulation of micro-organisms
Climate change is the greatest human induced environmental challenge ever faced by mankind (
Soils contain the world’s largest terrestrial stores of carbon, releasing ten times more CO2 than all anthropogenic emissions combined (
Members of the soil macrofauna may respond to future climate conditions by both “functional responses” and “numerical reponses”, in this paper used in a broad sense of changes in their activities which may alter their “function” in the ecosystem. Specifically we use aggregation as an example of a functional response. Secondly by “numerical responses” which are those responses of life history and population parameters that might influence the density and population dynamics of individual species.
Terrestrial isopods form a dominant component of the soil macrofauna in many ecosystems (
Aggregation is a behavioural adaption to avoid desiccation, where individuals group together to reduce water loss by creating a shell of higher relative humidy around the aggregate (
Microclimatic variables also strongly influence the numerical responses of isopods by affecting population characteristics such as, growth rate and survivorship (
We test the following hypotheses:
As relative humidity decreases aggregation and mortality rates will increase while growth rates will decrease.
As temperature increases aggregation, growth rates and mortality rates will all increase.
In the experiments on responses of aggregation behaviour to different temperatures and relative humidities five treatments were used: for responses to temperature 14, 17, 19, 21 or 23 °C and for responses to relative humidity 50, 60, 70, 80 or 90%. These ranges were chosen to bracket the range of microclimate conditions that might be encountered at the litter/soil interface of soils in south east England. 58 replicate arenas were used for each set of microclimate conditions. In both experiments Oniscus asellus was used as a representative of the Oniscidae and Porcellio scaber as a representive of the Porcellionidae for investigating responses of aggregation behaviour to temperature and Porcellio dilatatus as a representative of the Porcellionidae for investigating responses of aggregation to relative humidity.
O. asellus and P. dilatatus were also used to investigate responses of relative growth rate and mortality. A 2 × 2 factorial experimental design was used with temperatures of 18.5 °C and 13.5 °C and relative humidities of 90% and 70%. Each treatment combination was replicated 10 times. Differences in temperature of 5 °C, represent close to the higher predicted increases in air temperatures during the 21st century (
For investigating responses in aggregating behaviour to temperatures, base cultures of Oniscus asellus and Porcellio scaber were kept at 23 °C in the dark in 60 × 40 × 16 cm plastic containers with sloping bases of moist plaster of Paris from 0.5–4.0 cm deep covered with 6–2 cm sand to give a level surface with a moisture gradient along the length of the box and with pieces of bark for shelter and a mixture of leaves from broad leaved trees scattered over the sand surface for food. For investigating responses of aggregation to different relative humidities Oniscus asellus and Porcellio dilatatus base cultures were kept at 23 °C in the dark in 28 × 9 × 15.5 cm plastic containers with a base of 2 cm dampened plaster of Paris covered by 3cm sand and leaf litter. A mixture of broad leaved tree species provided food and cover. The boxes were sprayed with water at approximately 2 day intervals. For both experiments a soft paintbrush and a plastic weighing boat were used to transfer 10 individuals of a single species into 90 mm diameter Petri dishes divided into eight equal sections. Petri dish lids were replaced by a piece of nylon mesh (
Experimental arenas were transferred to and from the middle shelf of SANYO versatile environmental test chambers set to 90% RH for investigating responses to temperature and at 22 °C for investigating responses to relative humidity. Arenas were left for 20 minutes to allow arenas to equilibriate to experimental temperatures. They were then removed, photographed and the number of individuals in each section were counted. If an individual was on the dividing line between two segments it was recorded as in the section in which the largest percentage of its body was situated. If the individual was exactly half way over the boundary then it was recorded as being in the section in which the head end was situated (
The variance mean: ratio for numbers in segments was used as an index of aggregation. Aggregation indices were analysed in SPSS, using a two-way ANOVA, and Tukey post hoc comparison of means to compare species and humidities.
Three males and three females of both Oniscus asellus and Porcellio dilatatus, were divided into size classes and placed into a plastic container measuring 28 × 9 × 15.5 cm (
Containers were kept in SANYO versatile environmental test chambers and sprayed daily with the average mean summer rainfall of 1.65 mm (Moss and Hassall unpublished). The containers were kept in darkness for the full four weeks (
The growth rate was calculated using relative growth rate, RGR (
RGR = [log(LWt1)- log(LWt0)]/ T
where LWt0 is the live mass (mg) at the start of the experiment, LWt1 is the live mass four weeks later at the end of the experiment and T is the number of days from the start to the end of the experiment. The number of isopods of each species that died in each container was recorded weekly. Average values for growth rates in each container were used in the analyses to avoid pseudoreplication. The data were analysed using hree-way ANOVA in SPSS following testing for normality using the Kolmogorov-Smirnov test. Post hoc Tukey tests were used to compare different means. Mortality rates per week were analysed using the Mann Whitney U test as the data were not normally distributed.
Differences in aggregation under different microclimate conditions for both Oniscus asellus and Porcellio scaber varied significantly with temperature. For both species the most significant increase occurred between 14 and 17 °C (Fig.
Responses in aggregation index to differences in temperatures and relative humidity: Responses to different temperatures by a) Oniscus asellus, (F 4, 249 = 12.22; P < 0.001) and b) by Porcellio scaber (F4,249 = 3.76; P < 0.001). and to different relative humidies by c) Oniscus asellus, (F 4, 230 = 25.39; P < 0.001) and d) by Porcellio dilatatus (F4,171 = 16.85; P < 0.001). Means sharing the same letter are not significantly different from each other at P < 0.05.
In order to summarise results those for 17–23 °C were combined (average temperature 20 °C) for comparison with the significantly lower results for 14 °C. This showed that for O. asellus aggregation was 64% higher and for P. scaber 28% higher, following a 6 °C increase in temperature. Aggregation also changed significantly (P < 0.001) for both O. asellus and P. dilatatus at different relative humidities (Fig.
Aggregation of O. asellus increased by more than double the increase in aggregation shown by P. scaber for the same change in temperature. O. asellus also responded more to changes in relative humidity than P. scaber. Averaging the results for the two species by combining results for the two temperatures showed that for both species combined aggregation increased by 114% for a decrease of 25% in relative humidity (average value for F = 21.1) compared with a 46% increase in aggregation for a 6 °C rise in temperature (average value for F = 8.0).
Results of the 2 × 2 factorial experiment to investigate responses of growth and mortality to a 5 °C rise in temperature and a 20% reduction in relative humidity for O. asellus and P. dilatatus are shown in Fig.
Responses of relative growth rates to temperature and relative humidity. Responses to differences in temperature by a) Oniscus asellus, (F1, 36 = 0.905, P = 0.348) and. b) by Porcellio dilatatus, (F1, 36 = 5.112, P = 0.030); to differences in relative humidity of c) Oniscus asellus, (F1, 36 = 17.125, P < 0.001) and d) Porcellio dilatatus, (F1, 36 = 84.326, P < 0.001). Asterisks denote differences signficance at P < 0.05.
Similarly for mortality for one of the four combinations of species and relative humidity (P. dilatatus at 70% RH) was there a significant difference between 13.5 and 18.5 °C (Fig.
Response of mortality to temperature and relative humidity. Responses to temperature by a) Oniscus asellus, (U = 3097.0, P = 0.640. and b) by Porcellio dilatatus, (U = 2254.5, P = 0.016) and to relative humidity by c) Oniscus asellus (U = 1851.5, P < 0.001) and d) by Porcellio dilatatus (U = 2277.5 P < 0.001). Asterisks denote differences signficance at P < 0.05.
In this paper we use a reductionist, experimental approach to evaluate different responses to components of climate change. Specifically we address the question: will responses to climate change by soil animals indirectly help to mitigate the direct effects of increased soil temperatures increasing microbial activity and hence microbially mediated CO2 emissions? These direct responses of micro-organisms to a change in global temperatures could potentially cause a positive feedback between increased atmospheric CO2 concentrations, increased greenhouse effects, and increases in soil temperature and microbial metabolism (
While predictions of above ground temperature and rainfall patterns are reaching a sophisticated level of both spatial and temporal resolution (
Isopods are used as model arthropod macro-decomposers because their physiological, behavioural and ecological responses to different microclimates are well known (
The experimental animals responded to both an increase in temperature from 14 to 20 °C and a reduction of 25% in relative humidity by increasing the degree of aggregation, as found over other temperature and relative humidity ranges (
Both growth and mortality rates responded consistently more to a 20% decrease in relative humidy than to a 5 °C increase in temperature. In three of the four species × humidity treatments growth rates did increase over this range of temperature, as would be expected from previous studies of isopod growth rates (
In conclusion the answer to the question of whether the net functional and numerical responses of these model arthropod macro-decomposers will have a negative effect on the potential positive feedback between increased soil temperatures, increased soil CO2 emissions increasing greenhouse warming and hence further soil warming, will vary with regional differences in future rainfall patterns. In regions predicted to experience significant decreases in levels or periodicity of rainfall, the functional role of the animals in stimulating the micro-organisms is likely to be reduced. This can be predicted to partly mitigate against the potential positive feedback that could lead to increased CO2 emissions from soils.
We thank Alice Milton, Rob Sinclair, Morgen Dunn and Rory Tovell, for assistance with data collection, and Emma Hooper and Lydia Turner for technical support.