Research Article |
Corresponding author: Terézia Horváthová ( terezia.horvathova@uj.edu.pl ) Academic editor: Jasna Štrus
© 2015 Terézia Horváthová, Andrzej Antol, Marcin Czarnoleski, Paulina Kramarz, Ulf Bauchinger, Anna Labecka, Jan Kozłowski.
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:
Horvathova T, Antol A, Czarnoleski M, Kramarz P, Bauchinger U, Labecka A, Kozłowski J (2015) Does temperature and oxygen affect duration of intramarsupial development and juvenile growth in the terrestrial isopod Porcellio scaber (Crustacea, Malacostraca)? ZooKeys 515: 67-79. https://doi.org/10.3897/zookeys.515.9353
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According to the temperature-size rule (TSR), ectotherms developing under cold conditions experience slower growth as juveniles but reach a larger size at maturity. Whether temperature alone causes this phenomenon is unknown, but oxygen limitation can play a role in the temperature-size relationship. Oxygen may become limited under warm conditions when the resulting higher metabolism creates a greater demand for oxygen, especially in larger individuals. We examined the independent effects of oxygen concentration (10% and 22% O2) and temperature (15 °C and 22 °C) on duration of ontogenic development, which takes place within the maternal brood pouch (marsupium), and juvenile growth in the terrestrial isopod common rough woodlouse (Porcellio scaber). Individuals inside the marsupium undergo the change from the aqueous to the gaseous environment. Under hypoxia, woodlice hatched from the marsupium sooner, but their subsequent growth was not affected by the level of oxygen. Marsupial development and juvenile growth were almost three times slower at low temperature, and marsupial development was longer in larger females but only in the cold treatment. These results show that temperature and oxygen are important ecological factors affecting developmental time and that the strength of the effect likely depends on the availability of oxygen in the environment.
Temperature-size rule, Oxygen, Ontogenic development, Crustacea , Oniscidea
One of the most widespread patterns in biology is the temperature-size rule (TSR), which predicts slower growth and larger adult size for ectotherms growing in cold environments (
Growth rate of crustaceans is affected by the combination of internal and external factors (
Common rough woodlice (P. scaber) were collected in the autumn of 2013 in Kraków, Poland. Adult males and females were kept in separate plastic boxes (205 × 150 × 97 mm) in a temperature-controlled room at 15 °C (12-h day) and 8 °C (12-h night). The bottoms of the boxes were covered with wet sand and pieces of a clay pot were provided as shelter, and the animals were supplied ad libitum with alder and ash leaves collected from a nearby forest. After two weeks in these conditions, males (n = 1120) and females (n = 1400) were combined and transferred to new boxes for copulation and egg-laying. Fifty females and forty males were placed in each box and distributed among the experimental conditions. The photoperiod was changed to 16 h L:8 h D to initiate reproduction (
Animals were reared in two climate chambers (15 °C and 22 °C, POL-EKO APARATURA, Sp.j., Poland), which contained two plexi-chambers (40 × 50 × 55 cm, YETI – Agencja Reklamy, Poland) with either normoxic (22%) and hypoxic (10%) conditions. This experimental set-up gave us four temperate and oxygen combinations: 15 °C and 22% oxygen, 15 °C and 10% oxygen, 22 °C and 22% oxygen, and 22 °C and 10% oxygen. Oxygen levels were regulated (ROXY-4 four channel gas regulator, Sable Systems Europe GmbH, Germany) using oxygen (normoxic) or nitrogen gas (hypoxic), and the gases were provided by Air Products Sp. z o.o., Poland. Relative humidity was maintained at 75% by a separate dew point generator for each of the four environmental conditions (DG-4, Sable Systems Europe GmbH, Germany), and temperature and relative humidity settings were confirmed with Hygrochron iButtons (Maxim/Dallas Semiconductor, USA). The relative humidity inside the rearing boxes reached 98%, which was the humidity measured in the wild colony of isopods in Kraków.
Once per week, females were checked for the presence of a marsupium. Gravidity in P. scaber is characterised by the formation of a brood pouch on the ventral side of the body, and inside the marsupium, offspring undergo twenty discrete intramarsupial stages (
Statistical analysis was performed with R software (R Core Team 2014), and the graphs were made using Statistica10 (StatSoft, Inc. 2011). Prior to analysis, normality and the homogeneity of variance were checked; based on the type of data female post-parturial mass and duration of marsupial development data were logarithmically and square root transformed, respectively.
The duration of marsupial development was analysed by ANCOVA with oxygen and temperature as fixed factors and the mass of the mother as numeric covariate, and all possible interactions. In total, 401 gravid females were used in the analyses (22 °C normoxia, n = 99; 22 °C hypoxia, n = 49; 15 °C normoxia, n = 153; 15 °C hypoxia n = 100). The best model was obtained following stepwise removal of all non-significant interactions (temperature × oxygen, oxygen × maternal mass and oxygen × temperature × maternal mass).
Juvenile growth was analysed with a generalised linear mixed model (GLMM); oxygen, temperature and time since leaving the marsupium were fixed factors, and box number was a random factor. Juvenile mass data were transformed with natural logarithms. In total, we analysed 369 clutches (22 °C normoxia, n = 145; 22 °C hypoxia, n = 53; 15 °C normoxia, n = 100; 15 °C hypoxia, n = 71). All non-significant interactions (temperature × oxygen, oxygen × time and oxygen × temperature × time) were removed in a stepwise manner from the model and were not included in the final analysis.
Females reared in hypoxia released their offspring from their marsupia significantly sooner than females under normoxia (15 °C: 59.3 days normoxia, 56.8 days hypoxia; 22 °C: 23.1 days normoxia, 22.4 days hypoxia; p = 0.019; Table
Effects of temperature and oxygen on the length of marsupial development (ANCOVA) and juvenile mass (GLMM) in the isopod Porcellio scaber. Female post-parturial mass and juvenile mass were logarithmically transformed, and the duration of intramarsupial development was square-root transformed.
Effect | Df | F | p |
---|---|---|---|
Duration of intramarsupial development | |||
Temperature | 1 | 0.3 | 0.568 |
Oxygen | 1 | 5.6 | 0.019 |
Female post-parturial mass | 1 | 28.1 | < 0.0001 |
Temperature × female post-parturial mass | 1 | 13.7 | < 0.001 |
Error | 393 | ||
Juvenile mass | |||
Temperature | 1 | 1205.2 | < 0.0001 |
Oxygen | 1 | 3.5 | 0.064 |
Time | 1 | 2700.8 | < 0.0001 |
Temperature x time | 1 | 174.9 | < 0.0001 |
Juveniles grew faster in warm than in cold temperatures as indicated by the significant interaction between temperature and time (p < 0.0001; Table
We found that the duration of intramarsupial development of woodlice depended on temperature and oxygen level, with the latter effect being small, but statistically significant. Juvenile growth depended on temperature with a marginally significant effect of the level of oxygen (p = 0.064). Woodlice exposed to hypoxia completed their marsupial development sooner, and despite the shorter developmental time, juveniles under hypoxia were consistently slightly larger at both temperatures and time periods (after 9 and 13 weeks). However, because the difference was not significant, we can only conservatively state that hypoxia does not slow juvenile growth. Low temperature extended marsupial development and retarded juvenile growth; the two processes were almost two / three times slower at 15 °C than at 22 °C. Different behavioural, physiological and biochemical mechanisms may explain these patterns. For example, individuals in low temperature may just have reduced their food intake (
The shortened development time under warm conditions in P. scaber is consistent with the experimental evidence of faster development at high temperatures in a variety of crustacean species (
The observed effects of differential oxygen between the rate of marsupial development on one hand and juvenile growth on the other may be related to dissimilar oxygen availability in the aqueous and gaseous environments. The early development of isopods, as well as those of other crustacean groups (e.g., Amphipoda and Mysidacea), occurs in a fluid-filled brood pouch, which protects the early stages of development against desiccation, osmotic stress and mechanical damage (
The duration of intramarsupial development was not only affected by temperature and oxygen, but also by female mass; in the cold temperature, larger females incubated their progeny longer. Longer marsupial development in larger females agrees with findings for other species of terrestrial isopods: Armadillidium vulgare, Cylisticus convexus and P. scaber (
Our data show that oxygen level affects duration of intramarsupial development of the terrestrial isopod P. scaber in an unexpected way; development is shorter under lower levels of oxygen. Although we cannot exclude the possibility that mancae hatched sooner at earlier developmental stage compared to mancae in normoxia, our results suggest that oxygen availability is crucial for development in marsupium, and future studies may be directed towards determining the developmental stages of freshly hatched mancae reared in different experimental conditions. Our results further suggest that oxygen level rather does not affect growth rate after hatching. The size of the mother may affect the rate of embryonic development to some extent, but that effect depends on the thermal environment. Duration of intramarsupial development and early growth rate are accelerated in warm compared to cold environment. We might expect that such a strong effect on early life stages may have important consequences for subsequent life stages. To what extent our observed patterns may explain life-history strategies employed by terrestrial isopods living in different thermal environments and how this in turn may affect their range expansion and geographical distribution may provide interesting approach for future investigations.
This research was supported by a MAESTRO grant (2011/02/A/NZ8/00064). We thank Justyna Kierat for helping with the graphical presentation of the data and Karina Kapela and Ligia Kuriańska-Piątek for helping with the collection of the growth data. We also thank American Journal Experts for English corrections. We are grateful for the comments provided by the three anonymous reviewers that helped to improve the ms.