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Phenology and Growth Plasticity in a Short-Lived Chameleon Under Climatic Variation

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Phenology and Growth Plasticity in a Short-Lived Chameleon Under Climatic Variation SALAMANDRA 57(3): 435–443 Phenology and growth plasticity in a short-lived chameleon SALAMANDRA 15 August 2021 ISSN 0036–3375 German Journal of Herpetology Phenology and growth plasticity in a short-lived chameleon under climatic variation Miary Raselimanana1,2, Benjamin Rice3,4, Peter M. Kappeler5,6 & Falk Eckhardt5,7 1) Mention Zoologie et Biodiversité Animale, Faculté des Sciences, Université d’Antananarivo, BP 906, Antananarivo 101, Madagascar 2) Association Vahatra, BP 3972, Antananarivo 101, Madagascar 3) Department of Ecology and Evolutionary Biology, Princeton University, NJ 08544, USA 4) Madagascar Health and Environmental Research (MAHERY), Maroantsetra, Madagascar 5) Department of Sociology/Anthropology, Institute of Zoology and Anthropology, University of Göttingen, Kellnerweg 6, 37077 Göttingen, Germany 6) Behavioral Ecology and Sociobiology Unit, German Primate Center, Kellnerweg 4, 37077 Göttingen, Germany 7) Landkreis Celle, Amt für Umwelt und ländlicher Raum, Trift 29, 29221 Celle, Germany Corresponding author: Miary Raselimanana, e-mail: [email protected] Manuscript received: 14 May 2021 Accepted: 22 July 2021 by Jörn Köhler Abstract. Understanding species’ responses to climate change is crucial for the mitigation of its effects. Few studies, however, have examined how climate change impacts timing in reptile life cycles, or how it may interact with other life history traits. Here, we explore associations between climatic variation, reptile phenology, and juvenile growth. We used the chameleon spe- cies Furcifer labordi as a biological model given its unusual annual life history: embryonic diapause during austral winter is followed by synchronous hatching and an extremely short adult lifespan. We sampled chameleons (n = 674) and climate data across three field seasons between 2013–2018 in Kirindy Forest (CNFEREF), western Madagascar. Evidence of temperature and precipitation shifts have already been reported for this region. We show climate-dependent variation in the timing of hatching: it always occurred after the first rains and its onset varied by up to 32 days among years (equivalent to 12–17% of the total length of non-embryonic lifespan). Moreover, delayed rainy season onset resulted in a shortening of the period between the first rains and first hatching. Significant differences in hatching time and temperature also resulted in variation in juvenile growth, -spe cifically faster post-hatching growth in the late-hatching cohort. Therefore, climatic variation was associated with phenological and juvenile growth plasticity in the life cycle of F. labordi. Implications for conservation are worrying, as complete populations could be lost if a single cohort of this annual species cannot effectively respond to increasing climatic fluctuation. Key words. Squamata, Chamaeleonidae, Furcifer labordi, growth rate, hatching period, life history, phenological shift, western Madagascar. Introduction sex (e.g., Janzen & Paukstis 1991, Schwanz et al. 2010, Bal- len et al. 2016). Among vertebrates, poikilothermic taxa such as reptiles are In addition, range shifts due to climatic variation have been hypothesized to be particularly dependent on environmen- repeatedly documented in reptiles, including lizards (Houni- tal conditions for growth and reproduction. Together with et et al. 2009, Ceia-Hasse et al. 2014), snakes (Lourenço- their often-limited dispersal abilities, this constraint makes de-Moraes et al. 2019), and chelonians (Ihlow et al. 2012). reptiles particularly vulnerable to rapid environmental shifts, However, many populations now exist in isolated habitats and they may suffer higher extinction rates than other taxa without access to other potentially suitable habitats, making due to climatic change (Sinervo et al. 2010, Huey et al. range shifts an unlikely response to less favourable environ- 2012). In various reptiles, less dramatic effects of tempera- mental conditions. It is therefore important to better under- ture changes have been observed for hatchling phenotypes stand in situ responses to climatic variability across a wide (e.g., Booth 2006, Singh et al. 2020), hatchling behaviour range of taxa. Such information is interesting for understand- (Dayananda et al. 2017, Siviter et al. 2017), hatching suc- ing plasticity in life history traits and crucial for identifying cess (Díaz-Paniagua et al. 2006), post-hatching survival species threatened by climate change for ecological forecast- rate (Andrews et al. 2000), and, in some species, offspring ing and conservation planning (Akçakaya et al. 2006). © 2021 Deutsche Gesellschaft für Herpetologie und Terrarienkunde e.V. (DGHT), Germany Open access at https://www.salamandra-journal.com 435 Miary Raselimanana et al. Among in situ responses, modification of the timing of Materials and methods events in a life history can occur in response to abiotic fac- Study site and species tors exhibiting variation over time (e.g., temperature, pre- cipitation) (Bellard et al. 2012). Such phenological shifts The present study was carried out in the dry deciduous Kir- are well documented in many taxa (e.g., Stefanescu et al. indy Forest (CNFEREF) (44°28’–44°46’ E, 20°03’–20°10’ S, 2003, Rather et al. 2018, Stepanian & Wainwright 2018, 30–60 m a.s.l.), in the Harmonious Protected Landscape Staudinger et al. 2019). Studies focusing on reptiles’ phe- of Menabe Antimena, western Madagascar. Although orig- nological responses to climate change are scarce, but few inally covering 12,500 ha, the integrity of Kirindy Forest publications (e.g., Moreno-Rueda et al. 2009, Clarke & is currently threatened due to habitat loss and fragmenta- Zani 2012, Ljungström et al. 2015), focus on the shifts of tion (Goodman et al. 2018). The overall rate of deforesta- life history traits such as growth pattern caused by higher tion within the protected area was 0.67% per year with a ambient temperatures. maximum of 2.55% between 2008 and 2010 (Zinner et al. Here, we study variation in the phenology and growth 2014), presumably associated with the 2009 political crisis in annual cohorts of Labord’s chameleon (Furcifer labordi) in Madagascar. across years with significant climatic variation. This species Regarding local climatic conditions, the study area lies is characterized by an extreme life history among terrestri- in a transitional zone. The seasonally dry climate typical al vertebrates as it is thought to have the shortest lifespan of the west coast of Madagascar dominates in the north- (4–9 months) among tetrapods as part of an unusual an- ern part of the protected area. In contrast, the sub-arid cli- nual life cycle (Karsten et al. 2008, Eckhardt et al. 2019). mate typical of southwest Madagascar dominates in the These chameleons are almost exclusively represented in the southern portion (Goodman et al. 2018). Rainfall averages egg stage (embryonic diapause) during the austral win- 954mm per year (1981–2017), of which 96% falls between ter followed by synchronous hatching, extremely rapid November and April. Temperature ranges from a mean growth, and reproduction before the onset of the next dry daily minimum of 20.0°C to a mean daily maximum of season (Karsten et al. 2008). As an entire population con- 30.3°C. June to August is the coolest period (min, 12.4°C) sists of a single, synchronous age cohort, F. labordi provides and September to November the hottest (max. 33.4°C). Ki- a unique opportunity to monitor the effects of climate fluc- rindy Forest is characterized by intra-annual variation (i.e., tuations on phenology and growth for entire generations extreme seasonality) and unpredictable inter-annual var- of a tetrapod species. Further, due to the extremely com- iation in climate (Kappeler & Fichtel 2012), providing pressed lifespan, perturbations to timing could substan- an opportunity to study the effects of substantial climatic tially reduce the time window available for growth and re- changes over short time scales. production, raising questions about which components of the life history are more or less plastic. Furcifer labordi is restricted to dry forest patches in Vegetation cover measurement: western and southwestern Madagascar and is classified as Normalized Difference Vegetation Index (NDVI) Vulnerable in the IUCN Red List (IUCN 2021). Two pop- ulations have been studied: a northern population in Ki- NDVI, calculated by the reflection rate of red light (RED) rindy Forest, within the protected area of Menabe Anti- and near infrared light (NIR) [NDVI=(NIR−RED)/ mena (Eckhardt et al. 2017, 2019), and a southern pop- (NIR+RED)], is strongly correlated with aboveground net ulation in the protected area of Ranobe (Karsten et al. primary productivity (Myneni et al. 1995; see also http:// 2008). Here, we focus on the northern population from daacmodis.ornl.gov). Here, NIR and RED are the rates of Kirindy, where the abundance of F. labordi is still high near infrared light and red light that are reflected by the (Randrianantoandro et al. 2010) and the effects of cli- vegetation and recorded by the satellite sensor. The for- mate change have already been observed. Goodman et al. mula results from the fact that chlorophyll absorbs RED, (2018) analysed climatic fluctuations in the protected area whereas NIR is re-emitted. To compare seasons, we meas- of Menabe Antimena over 30 years (1985–2014). An annual ured the proportion of vegetation cover in the middle of increase of approximately 0.5% in precipitation has been the dry season (Jul.–Aug.), the late dry season (Sep.–Oct.),
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