The life cycle of the Neotropical water strider Telmatometra withei in different salinity environments

ABSTRACT Telmatometra withei (Bergroth, 1908) is a common water strider found across the Neotropics. Although, the taxonomy of T. withei is relatively well known, the specie’s life cycle has not been characterized. We use field surveys and laboratory experiments to describe the life cycle of two populations of T. withei in the Pacific coast of Panama. Specifically, we compared the life cycle between fresh and brackish water populations known to show local adaptation to each environment. We also contrast the life cycle of T. withei with that of other water striders previously reported in the literature. We found that the average life cycle of T. withei is approximately 66.7 days, and this period did not vary significantly between fresh (65.0 days) and brackish (68.3 days) populations. However, these estimates were longer than those reported for other species of water strides. In addition, traits associated with reproductive success such as egg length and fecundity varied significantly between populations, with females from freshwater populations showing larger values. This suggests that salinity can have important consequences for reproductive traits in T. withei, even if the overall life cycle may not be affected by salinity. Thus, characterizing the life history of these Neotropical organisms is crucial to understand the rich freshwater biodiversity of this region, as well as its response to both natural and anthropogenic disturbances.


Introduction
Telmatometra withei (Bergroth, 1908) is a widespread Neotropical water strider found from Ecuador to México, including Caribbean islands [1][2][3].Similar to other water striders, they inhabit the surface of the water [4,5], and are important aquatic predators, which play an important function in freshwater ecosystems [6][7][8][9][10].Although the taxonomy of T. withei is relatively well-known [1][2][3], the specie's life cycle remains undescribed.In addition, although water striders worldwide are well known for their ability to walk on the surface tension of the water, very few studies have described their life cycle [11,12], and to our knowledge, none has done so in Neotropical species.Thus, understanding the life cycle of T. withei will inform the life history of other water striders in Neotropical regions.More broadly, it will help appreciate other aspects of the hidden biodiversity present in Neotropical freshwater ecosystems [13].
Telmatometra withei is also widespread across the Isthmus of Panama [2,3], and it is found in a variety of habitats, including fresh (<0.5 ppt) and brackish (>1 ppt) water environments [14,15], with evidence for local adaptation to both environments [15].Salinity is also known to affect other aspects of T. withei, such in the case of the associated microbiome, which show overall higher diversity in brackish than freshwater populations [14,16].To our knowledge, however, the effect of salinity on the life cycle of T. withei has not been explored.Here, we describe, for the first time, the life cycle of two populations of T. withei inhabiting different salinity environments in the Pacific coast of Panama.

Material and methods
We collected individuals of T. withei from two sites located in Llano de Catival on the Western Azuero Peninsula on the Pacific coast of Panama.The first site is a freshwater site (Rio Negro, FW; 7°38'22.0"N, 80°58'36.6"O, Figure 1A), and the second is a brackish water site (Playa Reina lagoon, BW; 7°37"31.1" N, 81° 00"16.7"O, Figure 1B) [14,15].At both sites, we collected adult individuals using a standard D hand-net (mesh size: 500 μm).Individuals were transported in boxes to the laboratory where they were transferred to experimental boxes over a period of 90 days.The experimental boxes contained filtered water from the site of origin: FW (0 ppt) and BW (1 ppt).Specifically, the FW boxes contained water from Rio Negro (the CONTACT Anakena M. Castillo anakenamar@gmail.com"home" site of the FW population), and BW boxes contained water from Playa Reina lagoon (the "home" site for our BW population), following [15].
We used eight replicates of 10 individuals from each population (five females and five males).Sex was identified by direct observation of the genitalia.Individuals  were fed with eggs and adults of Drosophila [15].From experimental boxes, we recorded the following life history traits: pre-oviposition period, hatching time, nymph development time and total development time.We also recorded reproductive output, defined as the total number of eggs laid during the first 30 days of the experiment.In addition, we dissected 10 adult females from each FW and BW population collected in the field.From these individuals, we quantified the size, volume and number of eggs carried in their bodies (see Figure 2 for some typical developmental stages in T. withei).
Depending on sample sizes and the distribution of each trait, we implemented a combination of Student's t-test and Wilcoxon Signed Rank Test to test for differences in life history traits between FW and BW populations.Finally, to explore variation in the different life history stages in other water strides, we contrasted our results with data compiled from the published literature.All analyses were conducted in the R software [17].

Results
Overall, both freshwater (FW) and brackish water (BW) populations of T. withei showed a similar life cycle (Figure 3, Table 1).In particular, the duration of life stages such as pre-oviposition period and hatching time did not vary between populations (overall p > 0.05), and nymph development time only showed marginally significant differences (t (13) = −2.8;p = 0.05).Overall, total development time was 68.3 ± 8.1 and 65.0 ± 4.4 days for the FW and the BW population, respectively (Table 1).These estimates of developmental time appeared to be relatively longer, in contrast to previous life history estimates reported for other water strider species in different salinity environments (Table 2).
Egg volume and the number of eggs (obtained from dissected females) did not vary between populations (overall p > 0.05; Table 1).However, the total number of eggs laid in the experimental boxes (t [8] = −2.9;p = 0.05) and egg length (t [18] = −6.2;p = 0.001) was significantly larger in the FW population (Table 1).

Discussion
Our results showed that the life cycle of T. withei is approximately 66.7 days.This period is longer than previously reported for other species of water striders [12,19], and it did not vary significantly between our FW and BW populations from the Pacific coast of Panama.The only slight deviation from this later pattern was nymph development time, which appeared to be longer in the FW population, but this difference was only marginally statistically significant.This pattern is consistent with previous experimental estimates in the temperate water strider Aquarius paludum, which showed shorter life cycle [12,19] and nymph development time [12,20,21] than T. withei, but similar duration in both traits in FW and BW populations [12].Nymph development time (43.8 days) in our FW population of T. withei also tended to be longer than in FW populations of Gerris latiabdominis [11], but it seemed to be shorter than in the sea-water species Halobates matsumari, which present a wider range (40-50 days [22]).By contrast, the pre-oviposition period of T. withei appears to be shorter than the published estimates for both FW and BW populations of A. paludum [12,19,21].Thus, although salinity did not seem to alter the overall duration of the life cycle of our two populations of T. withei, salinity effects may vary by species, perhaps associated with geographical variation [12,19,[23][24][25] or other environmental factors.By contrast, we observed significant variation in traits associated with reproductive output between FW and BW populations.In particular, both egg length and fecundity (number of laid eggs) showed significantly higher averages in the FW than in the BW population.These results are consistent with our previous analyses that showed that salinity can affect traits associated with fitness in T. withei, including fecundity, survival, and overall reproductive success [15].This is also consistent with other studies showing that environmental stress (i.e.dry habitats) can affect reproductive traits in other species of water striders [18,20].For example, adults of A. paludum exposed to dry periods showed a decrease in the number of eggs laid [18].Thus, we suspect that a similar response could occur in T. withei exposed to different salinity levels.Although the actual mechanism by which salinity may be affecting reproductive output (but not total life cycle) in T. withei is unknown, one possibility is that the earlier stages of development are more sensitive to changes in salinity (e.g.present higher mortality) than juveniles or adult individuals.
One interesting field observation was an increase in the frequency of winged adults of T. withei in the BW population in comparison with the FW population (Figure 2D).This pattern has been observed previously in field collected individuals of T. withei [15], as well as in other water striders [12,19], and it is likely associated with adult dispersal in response to drastic changes in salinity [12,15,19].However, additional field surveys and experimental work are necessary to better quantify the frequency and persistence of these winged individuals of T. withei in different salinity environments.Further research is also needed to confirm if these winged individuals represent different morphotypes (i.e.stable sub-populations) within T. withei -as reported in other species [20], or if they indeed reflect developmental changes associated with changes in salinity [12,15,19].
Overall, our study represents the first characterization of the life cycle of the Neotropical water striders T. withei.Our results also suggest that salinity can be an important driver of variation in reproductive success in T. withei.As the global seal level continues to rise, understanding salinity effects on reproductive success and the life cycle of these freshwater organisms is crucial to predict the impact of salinization on freshwater biodiversity.Thus, we encourage further research to better understand the life cycle in additional populations of T. withei, as well as in other water strider species in Neotropical environments.Characterizing this basic aspect of the natural history of these organisms is crucial to understand the rich freshwater biodiversity of this region, as well as its response to both natural and anthropogenic disturbances.

Figure 3 .
Figure 3.Estimated life cycle of the water strider Telmatometra withei.Numbers of days represent the average value for each developmental stage in freshwater and brackish water populations (seeTable 1 for details).

Table 1
for details).

Table 1 .
Life history traits and reproductive output in the water strider Telmatometra withei.Values show the mean and standard error (±se) for each trait for both fresh and brackish water populations.Different letters represent statistically significant differences at p < 0.05.

Table 2 .
Estimated life history stages of water strider species in different salinity environments.Data were obtained from the published literature.