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Murillo-Rincon, A. P., Laurila, A. & Orizaola, G. (2017). Compensating for delayed hatching reduces offspring immune response and increases life-history costs. Oikos, 126(4), 565-571
Open this publication in new window or tab >>Compensating for delayed hatching reduces offspring immune response and increases life-history costs
2017 (English)In: Oikos, ISSN 0030-1299, E-ISSN 1600-0706, Vol. 126, no 4, p. 565-571Article in journal (Refereed) Published
Abstract [en]

Organisms are exposed to multiple sources of stress in nature. When confronted with a stressful period affecting growth and development, compensatory responses allow the restoration of individual fitness, providing an important buffering mechanism against climatic and other environmental variability. However, tradeoffs between increased growth/development and other physiological traits are predicted to prevent these high growth and development rates from becoming constitutive. Here, we investigated how compensatory responses in growth and development affect immune responses. By using low temperature to stop embryonic development, we exposed moor frog Rana arvalis tadpoles to two levels of time-constraints: non-delayed hatching and 12-day delayed hatching. In a common garden experiment, we recorded larval growth and development, as well as their immune response, measured as the inflammatory reaction after the injection of phytohaemagglutinin (PHA). Tadpoles originating from delayed hatching treatments had a lower immune response to PHA challenge than those from the non-delayed hatching treatment. In general, tadpoles from the delayed hatching treatment reached metamorphosis faster and at a smaller size than control tadpoles. However, immune-challenged tadpoles were not able to accelerate their development in response to delayed hatching. Our results indicate that 1) the innate immune response can be reduced in organisms undergoing compensatory developmental responses in growth and development and 2) compensatory capacity can be reduced when organisms are immunologically challenged. These dual findings reveal the complexity of handling multiple stressors and highlight the importance of examining the costs and limits of mounting an immune response in the context of increasing phenological instability ascribed to climate change.

National Category
Ecology
Identifiers
urn:nbn:se:uu:diva-321443 (URN)10.1111/oik.04014 (DOI)000398117500011 ()
Available from: 2017-05-05 Created: 2017-05-05 Last updated: 2017-05-31Bibliographically approved
Murillo-Rincon, A. P., Kolter, N. A., Laurila, A. & Orizaola, G. (2017). Intraspecific priority effects modify compensatory responses to changes in hatching phenology in an amphibian. Journal of Animal Ecology, 86(1), 128-135
Open this publication in new window or tab >>Intraspecific priority effects modify compensatory responses to changes in hatching phenology in an amphibian
2017 (English)In: Journal of Animal Ecology, ISSN 0021-8790, E-ISSN 1365-2656, Vol. 86, no 1, p. 128-135Article in journal (Refereed) Published
Abstract [en]

1. In seasonal environments, modifications in the phenology of life-history events can alter the strength of time constraints experienced by organisms. Offspring can compensate for a change in timing of hatching by modifying their growth and development trajectories. However, intra-and interspecific interactions may affect these compensatory responses, in particular if differences in phenology between cohorts lead to significant priority effects (i.e. the competitive advantage that early-hatching individuals have over late-hatching ones). 2. Here, we conducted a factorial experiment to determine whether intraspecific priority effects can alter compensatory phenotypic responses to hatching delay in a synchronic breeder by rearing moor frog (Rana arvalis) tadpoles in different combinations of phenological delay and food abundance. 3. Tadpoles compensated for the hatching delay by speeding up their development, but only when reared in groups of individuals with identical hatching phenology. In mixed phenology groups, strong competitive effects by non-delayed tadpoles prevented the compensatory responses and delayed larvae metamorphosed later than in single phenology treatments. Non-delayed individuals gained advantage from developing with delayed larvae by increasing their developmental and growth rates as compared to single phenology groups. 4. Food shortage prolonged larval period and reduced mass at metamorphosis in all treatments, but it did not prevent compensatory developmental responses in larvae reared in single phenology groups. 5. This study demonstrates that strong intraspecific priority effects can constrain the compensatory growth and developmental responses to phenological change, and that priority effects can be an important factor explaining the maintenance of synchronic life histories (i.e. explosive breeding) in seasonal environments.

Keywords
amphibians, compensatory growth, competition, development, life-history strategies, metamorphosis, phenology, synchrony
National Category
Zoology Developmental Biology Ecology
Identifiers
urn:nbn:se:uu:diva-313518 (URN)10.1111/1365-2656.12605 (DOI)000390325400014 ()
Funder
Helge Ax:son Johnsons stiftelse Swedish Research Council Formas, 2007-903
Available from: 2017-02-07 Created: 2017-01-20 Last updated: 2017-11-29Bibliographically approved
Orizaola, G. & Laurila, A. (2016). Developmental plasticity increases at the northern range margin in a warm-dependent amphibian. Evolutionary Applications, 9(3), 471-478
Open this publication in new window or tab >>Developmental plasticity increases at the northern range margin in a warm-dependent amphibian
2016 (English)In: Evolutionary Applications, ISSN 1752-4571, E-ISSN 1752-4571, Vol. 9, no 3, p. 471-478Article in journal (Refereed) Published
Abstract [en]

Accurate predictions regarding how climate change affects species and populations are crucial for the development of effective conservation measures. However, models forecasting the impact of climate change on natural environments do not often consider the geographic variation of an organism's life history. We examined variation in developmental plasticity to changing temperature in the pool frog (Pelophylax lessonae) across its distribution by studying populations from central areas (Poland), edge populations (Latvia) and northern marginal populations (Sweden). Relative to central and edge populations, northern populations experience lower and less variable temperature and fewer episodes of warm weather during larval development. Plasticity in larval life-history traits was highest at the northern range margin: larvae from marginal populations shortened larval period and increased growth rate more than larvae from central and edge populations when reared at high temperature. Maintaining high growth and development under the scarce spells of warm weather is likely adaptive for high-latitude populations. The detection of high levels of developmental plasticity in isolated, marginal populations suggests that they may be better able to respond to the temperature regimes expected under climate change than often predicted, reflecting the need to incorporate geographic variation in life-history traits into models forecasting responses to environmental change.

Keywords
climate change, ecological modelling, intraspecific variation, species distribution, temperature
National Category
Evolutionary Biology
Identifiers
urn:nbn:se:uu:diva-288610 (URN)10.1111/eva.12349 (DOI)000372406200006 ()26989438 (PubMedID)
Funder
Swedish Research Council Formas
Available from: 2016-05-04 Created: 2016-04-28 Last updated: 2017-11-30Bibliographically approved
Dijk, B., Laurila, A., Orizaola, G. & Johansson, F. (2016). Is one defence enough?: Disentangling the relative importance of morphological and behavioural predator-induced defences. Behavioral Ecology and Sociobiology, 70(2), 237-246
Open this publication in new window or tab >>Is one defence enough?: Disentangling the relative importance of morphological and behavioural predator-induced defences
2016 (English)In: Behavioral Ecology and Sociobiology, ISSN 0340-5443, E-ISSN 1432-0762, Vol. 70, no 2, p. 237-246Article in journal (Refereed) Published
Abstract [en]

Many organisms show predator-induced behavioural and morphological phenotypic plasticity. These defence mechanisms are often expressed simultaneously. To estimate the relative importance of these two defences, we conducted a laboratory experiment using tadpoles of the common frog (Rana temporaria) as prey and Aeshna dragonfly larvae as predators. We first raised tadpoles in the presence and absence of caged predators to induce differences in defensive morphology, and then conducted free ranging predator trials in environments that were either with or without the presence of predation cues to induce differences in defensive behaviour. This 2 x 2 design allowed us to separate the effects of inducible morphology from inducible behaviour. Caged predators induced deeper bodies and tailfins and reduced activity levels in tadpoles. The time to first capture was shortest in tadpoles without morphological or behavioural defences. Tadpoles with a behavioural defence had a significantly longer time to first capture. Tadpoles with only antipredator morphology tended to have a longer time to first capture as compared to those without any induced defences. This treatment also had a higher number of injured tadpoles as compared to other treatments, suggesting that inducible morphology facilitates predator escape due to the 'lure effect'. However, tadpoles with both behavioural and morphological defences did not have a longer time to first capture as compared to tadpoles with only morphological or behavioural induced defences. Our results suggest that both behavioural and morphological antipredator responses contribute to reduced capture efficiency by predators, but their simultaneous expression did not have any additive effect to the time of first capture and survival, and that the morphology response is most effective when tadpoles are active.

Keywords
Morphological defence, Phenotypic plasticity, Antipredator behaviour, Rana temporaria
National Category
Developmental Biology
Identifiers
urn:nbn:se:uu:diva-277774 (URN)10.1007/s00265-015-2040-8 (DOI)000368633900002 ()
Funder
Swedish Research Council
Available from: 2016-02-23 Created: 2016-02-23 Last updated: 2017-11-30Bibliographically approved
Orizaola, G. & Valdés, A. E. (2015). Free the tweet at scientific conferences [Letter to the editor]. Science, 350(6257), 170-U149
Open this publication in new window or tab >>Free the tweet at scientific conferences
2015 (English)In: Science, ISSN 0036-8075, E-ISSN 1095-9203, Vol. 350, no 6257, p. 170-U149Article in journal, Letter (Refereed) Published
National Category
Biological Sciences
Identifiers
urn:nbn:se:uu:diva-266217 (URN)10.1126/science.350.6257.170-c (DOI)000362405600025 ()26450202 (PubMedID)
Available from: 2015-11-05 Created: 2015-11-05 Last updated: 2017-12-01Bibliographically approved
Orizaola, G. & Valdés, A. E. (2015). Redes Sociales para el Desarrollo Científico [Letter to the editor]. The Information and Scientific News Service (SINC)
Open this publication in new window or tab >>Redes Sociales para el Desarrollo Científico
2015 (Spanish)In: The Information and Scientific News Service (SINC)Article in journal, Letter (Other (popular science, discussion, etc.)) Published
Place, publisher, year, edition, pages
Agencia SINC: , 2015
National Category
Media and Communications
Identifiers
urn:nbn:se:uu:diva-287503 (URN)
Available from: 2016-04-25 Created: 2016-04-25 Last updated: 2016-04-25Bibliographically approved
Orizaola, G., Dahl, E. & Laurila, A. (2014). Compensatory growth strategies are affected by the strength of environmental time constraints in anuran larvae. Oecologia, 174(1), 131-137
Open this publication in new window or tab >>Compensatory growth strategies are affected by the strength of environmental time constraints in anuran larvae
2014 (English)In: Oecologia, ISSN 0029-8549, E-ISSN 1432-1939, Vol. 174, no 1, p. 131-137Article in journal (Refereed) Published
Abstract [en]

Organisms normally grow at a sub-maximal rate. After experiencing a period of arrested growth, individuals often show compensatory growth responses by modifying their life-history, behaviour and physiology. However, the strength of compensatory responses may vary across broad geographic scales as populations differ in their exposition to varying time constraints. We examined differences in compensatory growth strategies in common frog (Rana temporaria) populations from southern and northern Sweden. Tadpoles from four populations were reared in the laboratory and exposed to low temperature to evaluate the patterns and mechanisms of compensatory growth responses. We determined tadpoles' growth rate, food intake and growth efficiency during the compensation period. In the absence of arrested growth conditions, tadpoles from all the populations showed similar (size-corrected) growth rates, food intake and growth efficiency. After being exposed to low temperature for 1 week, only larvae from the northern populations increased growth rates by increasing both food intake and growth efficiency. These geographic differences in compensatory growth mechanisms suggest that the strategies for recovering after a period of growth deprivation may depend on the strength of time constraints faced by the populations. Due to the costs of fast growth, only populations exposed to the strong time constraints are prone to develop fast recovering strategies in order to metamorphose before conditions deteriorate. Understanding how organisms balance the cost and benefits of growth strategies may help in forecasting the impact of fluctuating environmental conditions on life-history strategies of populations likely to be exposed to increasing environmental variation in the future.

Keywords
Adaptive plasticity, Climate change, Food intake, Growth efficiency, Growth rates, Time constraints
National Category
Natural Sciences
Identifiers
urn:nbn:se:uu:diva-218591 (URN)10.1007/s00442-013-2754-0 (DOI)000329624300013 ()
Available from: 2014-02-13 Created: 2014-02-13 Last updated: 2017-12-06Bibliographically approved
Nunes, A. L., Orizaola, G., Laurila, A. & Rebelo, R. (2014). Morphological and life-history responses of anurans to predation by an invasive crayfish: an integrative approach. Ecology and Evolution, 4(8), 1491-1503
Open this publication in new window or tab >>Morphological and life-history responses of anurans to predation by an invasive crayfish: an integrative approach
2014 (English)In: Ecology and Evolution, ISSN 2045-7758, E-ISSN 2045-7758, Vol. 4, no 8, p. 1491-1503Article in journal (Refereed) Published
Abstract [en]

Predator-induced phenotypic plasticity has been widely documented in response to native predators, but studies examining the extent to which prey can respond to exotic invasive predators are scarce. As native prey often do not share a long evolutionary history with invasive predators, they may lack defenses against them. This can lead to population declines and even extinctions, making exotic predators a serious threat to biodiversity. Here, in a community-wide study, we examined the morphological and life-history responses of anuran larvae reared with the invasive red swamp crayfish, Procambarus clarkii, feeding on conspecific tadpoles. We reared tadpoles of nine species until metamorphosis and examined responses in terms of larval morphology, growth, and development, as well as their degree of phenotypic integration. These responses were compared with the ones developed in the presence of a native predator, the larval dragonfly Aeshna sp., also feeding on tadpoles. Eight of the nine species altered their morphology or life history when reared with the fed dragonfly, but only four when reared with the fed crayfish, suggesting among-species variation in the ability to respond to a novel predator. While morphological defenses were generally similar across species (deeper tails) and almost exclusively elicited in the presence of the fed dragonfly, life-history responses were very variable and commonly elicited in the presence of the invasive crayfish. Phenotypes induced in the presence of dragonfly were more integrated than in crayfish presence. The lack of response to the presence of the fed crayfish in five of the study species suggests higher risk of local extinction and ultimately reduced diversity of the invaded amphibian communities. Understanding how native prey species vary in their responses to invasive predators is important in predicting the impacts caused by newly established predator-prey interactions following biological invasions.

Keywords
Crayfish, integration of responses, invasive species, phenotypic plasticity, tadpoles
National Category
Ecology
Identifiers
urn:nbn:se:uu:diva-225075 (URN)10.1002/ece3.979 (DOI)000334601100019 ()
Available from: 2014-06-19 Created: 2014-05-27 Last updated: 2017-12-05Bibliographically approved
Nunes, A. L., Orizaola, G., Laurila, A. & Rebelo, R. (2014). Rapid evolution of constitutive and inducible defenses against an invasive predator. Ecology, 95(6), 1520-1530
Open this publication in new window or tab >>Rapid evolution of constitutive and inducible defenses against an invasive predator
2014 (English)In: Ecology, ISSN 0012-9658, E-ISSN 1939-9170, Vol. 95, no 6, p. 1520-1530Article in journal (Refereed) Published
Abstract [en]

Invasive alien predators can impose strong selection on native prey populations and induce rapid evolutionary change in the invaded communities. However, studies on evolutionary responses to invasive predators are often complicated by the lack of replicate populations differing in coexistence time with the predator, which would allow the determination of how prey traits change during the invasion. The red swamp crayfish Procambarus clarkii has invaded many freshwater areas worldwide, with negative impacts for native fauna. Here, we examined how coexistence time shapes antipredator responses of the Iberian waterfrog (Pelophylax perezi) to the invasive crayfish by raising tadpoles from five populations differing in historical exposure to P. clarkii (30 years, 20 years, or no coexistence). Tadpoles from non-invaded populations responded to the presence of P. clarkii with behavioral plasticity (reduced activity), whereas long-term invaded populations showed canalized antipredator behavior (constant low activity level). Tadpoles from one of the long-term invaded populations responded to the crayfish with inducible morphological defenses (deeper tails), reflecting the use of both constitutive and inducible antipredator defenses against the exotic predator by this population. Our results suggest that, while naive P. perezi populations responded behaviorally to P. clarkii, the strong predation pressure imposed by the crayfish has induced the evolution of qualitatively different antipredator defenses in populations with longer coexistence time. These responses suggest that strong selection by invasive predators may drive rapid evolutionary change in invaded communities. Examining responses of prey species to biological invasions using multiple populations will help us better forecast the impact of invasive predators in natural communities.

Keywords
coexistence time, invasive predator, Pelophylax perezi, plastic and constitutive defenses, population, predator recognition, Procambarus clarkii, rapid evolution
National Category
Ecology
Identifiers
urn:nbn:se:uu:diva-228543 (URN)10.1890/13-1380.1 (DOI)000337218500011 ()
Available from: 2014-07-17 Created: 2014-07-16 Last updated: 2017-12-05Bibliographically approved
Richter-Boix, A., Orizaola, G. & Laurila, A. (2014). Transgenerational phenotypic plasticity links breeding phenology with offspring life-history. Ecology, 95(10), 2715-2722
Open this publication in new window or tab >>Transgenerational phenotypic plasticity links breeding phenology with offspring life-history
2014 (English)In: Ecology, ISSN 0012-9658, E-ISSN 1939-9170, Vol. 95, no 10, p. 2715-2722Article in journal (Refereed) Published
Abstract [en]

The timing of seasonal life-history events is assumed to evolve to synchronize life cycles with the availability of resources. Temporal variation in breeding time can have severe fitness consequences for the offspring, but the interplay between adult reproductive decisions and offspring phenotypes remains poorly understood. Transgenerational plasticity (TGP) is a potential mechanism allowing rapid responses to environmental change. Here, we investigated if experimentally delayed breeding induces TGP in larval life-history traits in the moor frog (Rana arvalis). We found clear evidence of TGP in response to changes in breeding phenology: delayed breeding increased offspring development and growth rates in the absence of external cues. This constitutes the first unequivocal evidence for TGP in response to changes in breeding phenology in vertebrates. TGP can play an important role in adjusting offspring life-history strategies to the environment they are most likely to encounter, and may constitute an important mechanism for coping with climate change.

Keywords
climate change, complex life-cycles, life-history strategies, metamorphosis, seasonal clocks, timing of reproduction
National Category
Ecology Zoology
Identifiers
urn:nbn:se:uu:diva-238587 (URN)10.1890/13-1996.1 (DOI)000344317300005 ()
Available from: 2014-12-16 Created: 2014-12-14 Last updated: 2017-12-05Bibliographically approved
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ORCID iD: ORCID iD iconorcid.org/0000-0002-6748-966X

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