Research Article |
Corresponding author: J. Carlos Alvarado-Avilés ( jalvaradoa@uaemex.mx ) Academic editor: Johannes Foufopoulos
© 2024 Hermilo Sánchez-Sánchez, Adriana Jocelyn Morales-Gonzaga, Ken Oyama, J. Carlos Alvarado-Avilés.
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:
Sánchez-Sánchez H, Morales-Gonzaga AJ, Oyama K, Alvarado-Avilés JC (2024) Reproductive effort of Plestiodon copei (Squamata, Scincidae), a highland viviparous lizard from Central Mexico. Herpetozoa 37: 1-10. https://doi.org/10.3897/herpetozoa.37.e111749
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Female reproductive effort is defined as the proportion of total energy or resources devoted to reproduction. In reptiles, there is frequently high inter- and intra-population variation related to several factors, such as food availability, climatic conditions, age and size, all of which, in turn, also influence survival and future reproduction. The present study is the first reproductive effort analysis of a population of the high-mountain scincid lizard Plestiodon copei in central Mexico, focusing on relative litter mass (RLM), investment per capita (INV) and productivity (PROD). We also compared the reproductive efficacy of P. copei to those of other Mexican congeners. We collected 24 gravid females of P. copei over a 4-year period and recorded a total of 90 neonates born in captivity. We found significant variation in neonatal mass amongst individual females and across years. We recorded an average litter size of 3.75 and an average litter mass of 1.25 g, which were positively correlated with both the size and total mass of the reproductive females. The RLM, INV and PROD values (0.301, 0.428 g and 1.236 g × year-1, respectively) for P. copei were greater than those for other Mexican species in the P. brevirostris group (0.290, 0.412 g and 1.135 g × year-1), revealing that females of P. copei from Tenango invest a comparatively high amount of their resources in reproduction.
life history, litter mass, litter size, reproductive investment, skink lizard, Trans-Mexican Volcanic Belt
Reproductive investment is a central aspect of the theory of life history evolution, which states that an individual must allocate an optimal proportion of its available energy to reproduction which, in turn, will be reflected in statistics, such as in neonate/egg size and mass, litter/clutch size and mass and reproductive effort (
Female lizards can also exhibit remarkable inter- and intraspecific variations in their reproductive life history traits (Cruz-Elizalde and Ramírez-Bautista 1998;
In the mountainous regions of Mexico, several studies have analysed the reproductive strategies utilised in different genera of lizards, such as Barisia (
To estimate the reproductive investment of female reptiles, several indices have been developed that take into consideration the characteristics of both females and their progeny. Relative clutch mass/relative litter mass (RCM/RLM = fraction of female body mass devoted to reproduction) is the most frequently used index for estimating reproductive effort in lizards for both oviparous and viviparous species (
Plestiodon copei (Fig.
We collected 24 late-pregnant females of P. copei from March–early April 2014 to 2017 near Tenango del Valle (19°05'54.74"N, 99°38'26.43"W) at an elevation of ca. 3030 m in the TMVB of central Mexico. Gravid females of P. copei were identified in situ by their greater abdominal volume. All females were captured in a landscape dominated by pine forests (Pinus teocote, P. montezumae and P. rudis) and grasslands (Muhlenbergia macroura) and surrounded by agricultural fields (
We transported the collected females to the Laboratory of Genetic and Molecular Evolution (Universidad Autónoma del Estado de México) and individually housed them in plastic boxes (400 × 220 × 180 mm) with natural substrate (e.g. soil, gravel, mulch) and refuge objects (e.g. rocks and bark) obtained from the capture site. All females were maintained according to the thermal conditions described by
We recorded the snout–vent length (SVL) and the total mass (TM = female body mass before birth) of each gravid female after capture. Females were checked at least once per day for 2 to 3 weeks and weighed daily until parturition. After birth, the following data were immediately recorded: absolute mass (AM = female body mass after birth), litter size (LS = number of neonates produced by a female), litter mass (LM = sum of the masses of all neonates produced by a female) and mean litter mass (MLM = average mass of the neonates of each litter).
The reproductive effort of P. copei females was estimated as follows: (a) relative litter mass; RLM = LM/AM; (b) reproductive investment per capita; INV = (TM−AM)/LS; and (c) estimated productivity; PROD = (MLM × LS) × year-1 (
We checked all variables for normality using the Shapiro‒Wilk test and for the presence of outliers with box plots in SPSS ver. 24 (
Twenty-four gravid females were captured over a 4-yr period. The SVL ranged from 51.8 mm to 69.0 mm and the mean size was 62.711 mm (SD = 4.141 mm, CV = 6.6%, n = 24). In captivity, the females gave birth to a total of 90 neonates (range = 2−5 neonates per litter, mean = 3.750, SD = 0.897, CV = 23.9%) from mid-April to the last week of June. LMs ranged from 0.659 g to 1.844 g (mean = 1.250 g, SD = 0.310, CV = 31.2%, n = 24), while MLMs ranged from 0.256 g to 0.405 g (mean = 0.330 g, SD = 0.033, CV = 10.0%, n = 24).
For P. copei, the estimated range for RLM was 0.129−0.530 (mean = 0.301, SD = 0.094, CV = 31.2%, n = 24), the range for INV was 0.190−0.694 g (mean = 0.428 g, SD = 0.103, CV = 24.1%, n = 24) and the range for PROD was 0.659−1.844 g × year-1 (mean = 1.236 g × year-1, SD = 0.326, CV = 26.4%, n = 24).
Correlation analyses revealed significant positive correlations between female SVL and LS (r = 0.427, R2 = 0.182, F1,23 = 4.903, p = 0.037) and LM (r = 0.458, R2 = 0.210, F1,23 = 5.851, p = 0.024) (Fig.
In several lizard species, reproductive investment has been shown to be associated with phenotypic and physiological traits, both of which are optimised by natural selection (
The gravid females varied in both SVL and TM; these variables, in turn, showed significant correlations with litter size and litter mass.
The timing of birth in captivity for these study animals was consistent with the birth period reported by
The minimum gravid female sizes reported here indicate that Tenango females can reach sexual maturity at relatively small body sizes (SVL = 51.8 mm), as the SVL of the smallest pregnant female previously reported was 56.0 mm (
It has been shown that, particularly for ectothermic species living at high elevations, temperature is an important factor shaping life history strategies, as well as determining growth rate and age and size at sexual maturity (
The effects of temperature on determining the size of females of P. copei at sexual maturity are similar to those of other high-mountain lizards, such as Mediodactylus heterocercus and Darevskia derjugini. In all three lizard species, sexually mature females with smaller minimum body sizes were encountered under relatively warm temperature conditions, while sexually mature females with larger minimum sizes were found in comparatively cooler environments. (
The mass of the offspring is another reproductive characteristic of P. copei that, if influenced by environmental temperature, suggests a rapid life history strategy for Tenango animals. According to the PROD index, the total mass of offspring produced in a year is greater in Tenango than in San Lorenzo Acopilco. This pattern is similar to that observed in another temperate-adapted skink species, Eulamprus tympanum (
Our analysis of the masses of individual P. copei neonates revealed marked differences both within and between litters (see Fig.
Moreover, the differences in MLM observed between years suggest that there are other factors that could influence the reproductive investment of P. copei females in Tenango. Possible factors include differences in the SVL of females or in environmental conditions, such as temperature variation and food availability (
However, the lower MLMs recorded since 2015 could be attributed to reduced food availability, as the collection site showed repeated signs of human-caused grass fires due to traditional agricultural and grazing activities that allowed fires to spread into the forest. This type of vegetation disturbance has been shown – due to the lethal surface temperatures caused by fire – to negatively impact the abundance of ground-dwelling beetles which, in turn, are an important food source for P. copei (
In conclusion, by comparing the RLM, INV and PROD indices used to evaluate reproductive effort, we observed that P. copei had slightly greater values than the mean estimated for species in the P. brevirostris group (Table
Reproductive effort estimations for several Mexican species of Plestiodon.
Species | Location | RCM / RLM | INV (g) | PROD (g × year-1) | Reference |
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Plestiodon bilineatus (n = 1) | Valparaíso, Zacatecas | – | – | 1.820 |
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Plestiodon sp. PT* (n = 7) | Volcán La Malinche, Tlaxcala | 0.231 | 0.432 | 0.850 |
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Plestiodon sp. PT*(n = 17) | Chilchota, Puebla | 0.334 | 0.325 | 1.168 |
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Plestiodon sp. OX* (n = 1) | Santa Inés del Monte, Oaxaca | – | 0.515 | 1.240 |
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P. indubitus (n = 1) | Sur de Tres Marías, Morelos | – | – | 0.640 |
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P. copei (n = 3) | San Lorenzo Acopilco, CDMX | – | – | 1.020 |
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P. copei (n = 24) | Tenango, Estado de México | 0.301 | 0.428 | 1.236 | This study |
P. dicei (n = 1) | Pablillo, Nuevo León | – | – | 1.212 |
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P. dicei (n = 1) | San Antonio de las Alazanas, Coahuila | – | – | 1.164 |
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P. dugesii (n = 21) | Mazamitla, Jalisco | 0.292 | 0.362 | 1.001 |
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Averages | 0.290 | 0.412 | 1.135 |
The observations presented here suggest that the reproductive strategy of P. copei from Tenango may have been shaped by the prevailing extreme environmental conditions (
We thank to E. Carbajal and S. H. Cuadros for their assistance in the field. Collecting permits (SGPA/DGVS/08371/14) were provided by the Secretaría de Medio Ambiente y Recursos Naturales (SEMARNAT). We also thank the anonymous reviewers for comments and suggestions to the manuscript.
Games-Howell post-hoc multiple comparisons
Data type: xlsx
Mean monthly temperature based on 59 years of records (1951–2010) for four populations of Plestiodon copei
Data type: docx