natural mortality and hatching patterns
We observed a total of 22 533 eggs in 350 clutches from 2003–2005 (clutch size 64 ± 1·4 eggs). At Bridge Pond, only 14 ± 2% of eggs survived to hatch, whereas 46 ± 3% of eggs at Ocelot Pond hatched (Fig. 1). Eggs that failed to hatch died from desiccation, were eaten by terrestrial predators, failed to develop (presumably unfertilized), became submerged and were eaten by aquatic predators before the start of the third day, or became submerged and drowned (Fig. 1). In addition, some eggs disappeared underwater after the start of the third day; these may have hatched or been eaten, but their fate is unknown (Fig. 1).
Figure 1. Fates of Dendropsophus ebraccatus eggs monitored at two ponds in Panama from 2003–2005. Embryos either hatched, or died before hatching from egg desiccation, terrestrial predation, drowning, or aquatic predation after submergence. Some eggs did not develop, and were presumably unfertilized. Some disappeared underwater after hatching competence; these could have hatched or been eaten. N = 350 egg clutches. Data are mean proportion of affected eggs per clutch + SE.
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We frequently observed social wasps (P. rejecta and A. centralis) and ants (Azteca sp.) preying on eggs, and damage patterns corroborate that these were the most important predators, accounting for all but one instance of observed arboreal egg predation. Wasp predation often leaves yolk spilled on the leaf, especially when wasps prey on young embryos (Warkentin 2000). Wasps also remove embryos from the jelly, leaving empty egg jelly behind (Warkentin 2000). Ants generally remove eggs and jelly completely; we rarely observed this without also seeing ants on the clutch. Wasp predation was more widespread as wasps could reach clutches throughout the ponds, whereas Azteca only preyed upon eggs in the same plant as their nest. Leaf-cutter ants killed one clutch while harvesting leaves from a plant containing D. ebraccatus eggs. We saw no evidence of snake predation on D. ebraccatus egg clutches, although it is common on Agalychnis callidryas egg clutches at Ocelot Pond (Warkentin 2000) and has been reported for D. ebraccatus elsewhere (Donnelly & Guyer 1994). From predation experiments (J. Touchon unpublished), we know that fishes (A. ruberrimus and Brachyraphus sp.) and tadpoles (including conspecifics and Leptodactylus pentadactylus Laurenti) consume flooded eggs.
The amount of rainfall that clutches received during development varied greatly during our observation periods (range 0–179·8 mm, mean 33·3 ± 1·9 mm). The amount of rain that fell on clutches we observed was greater in 2005 than either 2003 or 2004, which did not differ from one another (2003 = 13·1 ± 0·98 mm, 2004 = 17·4 ± 1·6 mm, 2005 = 77·1 ± 3·7 mm; LM, F2,347 = 267·27, P < 0·0001; Tukey's comparisons, 2003–2004, P = 0·30, 2003–2005 and 2004–2005, P < 0·0001). In addition, dry days were more common during our 2003 and 2004 observation periods (proportion dry days: 2003 = 0·5, 2004 = 0·62, 2005 = 0·33). Mean daily temperature and relative humidity during our observations did not vary significantly between years, although 2005 was slightly cooler than 2003 or 2004 (2003 = 25·9 ± 0·2 °C, 2004 = 26·1 ± 0·1 °C, 2005 = 25·5 ± 0·2 °C; LM, temperature, F2,57 = 2·74, P = 0·073; humidity, F2,57 = 1·54, P = 0·22; data from ACP).
Clutches were laid farther above the water surface at Ocelot Pond than at Bridge Pond, and oviposition height did not vary across years (Ocelot = 62·1 ± 3·6 cm high, Bridge = 20·9 ± 1·9 cm high; LM, pond, F1,196 = 105·2, P < 0·0001; year, F1,196 = 0·09, P = 0·77). The mean thickness of egg clutches throughout development increased with increasing rainfall and differed between ponds, but did not differ across years (Fig. 2a; LM, overall model, F7,192 = 17·41, P < 0·0001; rainfall, F1,192 = 90·39, P < 0·0001; pond, F1,192 = 12·35, P = 0·0006; year, F 1,192 = 0·07, P = 0·80). The effect of rainfall on clutch thickness, however, differed between ponds and across years, as indicated by significant rainfall-by-pond and rainfall-by-year interactions (Fig. 2a; rainfall × pond, F1,192 = 6·40, P = 0·012; rainfall × year, F1,192 = 11·78, P = 0·0007).
Figure 2. Effects of rainfall on Dendropsophus ebraccatus eggs at two ponds in Panama. (a) Increasing rainfall increases clutch thickness, as the jelly surrounding embryos absorbs water (linear model, F1,192 = 90·39, P < 0·0001). This relationship is steeper at Ocelot Pond (open circles and dashed lines), where clutches are more shaded, than at Bridge Pond (closed circles and solid lines) (linear model, F1,192 = 12·35, P = 0·0006). Increasing rainfall decreases mortality from (b) desiccation and (c) terrestrial predators (ants and wasps). Mortality from desiccation decreases with increasing rainfall (generalized linear model, F1,348 = 34·94, P < 0·0001) and varies between ponds (F1,347 = 26·62, P < 0·0001) and across years (F2,345 = 4·74, P =0·009). Predation decreases with increasing rainfall (F1,348 = 20·46, P < 0·001) and varied across years (F2,345 = 13·45, P < 0·0001). Lines are predictions from (a) linear and (b and c) generalized linear models. Data points represent individual clutches monitored in the field. Clutch thickness is the average for each clutch across development, from twice-daily measurements. N = 200 clutches observed from 2004–2005 in (a) and 350 clutches observed from 2003–2005 in (b and c).
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As rainfall increased, mortality from desiccation decreased (Fig. 2b, Table 1) and mortality was less at Ocelot Pond than at Bridge Pond (Fig. 2b, Table 1). In addition, there was a significant effect of year; egg desiccation mortality was lower in 2005 than either 2003 or 2004 (proportion of eggs desiccated, 2003 = 0·38 ± 0·03, 2004 = 0·43 ± 0·04, 2005 = 0·23 ± 0·02). There were no interactions among rainfall, pond or year on egg mortality from desiccation (Table 1).
Table 1. Summaries of quasibinomial GLM's of Dendropsophus ebraccatus egg mortality from desiccation and predation at two ponds in Panama from 2003–2005. The total deviance of each model is shown, along with the proportion of deviance accounted for by each predictor variable. The proportion of the deviance explained in a quasibinomial GLM is analogous to an R2 in a linear regression. Significant variables are highlighted in bold
|Model||d.f.||Deviance||Deviance explained||F||P value|
|Desiccation|| ||17 505·7|| || || |
| Rainfall||1,348||1318·6||0·075||34·94||< 0·0001|
| Pond||1,347||1004·6||0·057||26·62||< 0·0001|
| Rainfall × Pond||1,344||18·5||0·001||0·49||0·48|
| Rainfall × Year||2,342||175·3||0·010||2·32||0·10|
| Pond × Year ||2,340||107·8||0·006||1·42||0·24|
| Rainfall × Pond × Year||3,338||34·7||0·002||0·45||0·63|
|Total deviance explained|| || ||0·172|| || |
|Predation|| ||14 023·3|| || || |
| Rainfall||1,348||673·8||0·048||20·46||< 0·0001|
| Year||2,345||885·7||0·063||13·45||< 0·0001|
| Rainfall × Pond||1,344||230·3||0·016||6·99||0·009|
| Rainfall × Year||2,342||231·7||0·016||3·52||0·031|
| Pond × Year ||2,340||181·3||0·013||2·75||0·065|
| Rainfall × Pond × Year||3,338||130·8||0·009||1·98||0·139|
|Total deviance explained|| || ||0·168|| || |
As rainfall on an egg clutch increased, predation from ants and wasps decreased (Fig. 2c; Table 1). There was no effect of pond on predation by ants and wasps, but predation did vary across years (Fig. 2c, Table 1; proportion eggs eaten by ants and wasps, 2003 = 0·35 ± 0·03, 2004 = 0·23 ± 0·03, 2005 = 0·11 ± 0·02). In addition, there were interactions between pond and rainfall, and year and rainfall, such that the effect of rain on decreasing predation was not the same at both ponds or across years (Fig. 2c, Table 1).
A lack of rainfall during the first 24 h after oviposition increased mortality of eggs at Bridge Pond approximately 10%, whereas it had no effect on mortality at Ocelot Pond (Fig. 3a; GLM, rain, F1,346 = 0·8, P = 0·38; pond, F1,346 = 66·4, P < 0·0001; rain × pond, F1,346 = 5·2, P = 0·024). No rainfall during the first 48 h, however, increased egg mortality at both ponds (Fig. 3b; GLM, F1,346 = 11·7, P = 0·0007; pond, F1,346 = 68·3, P < 0·0001; rain × pond, F1,346 = 12·2, P = 0·0005). Eggs that were not rained on for the first 48 h at Bridge Pond suffered 98 ± 1·3% mortality (Fig. 3b).
Figure 3. Timing of rainfall after oviposition affects Dendropsophus ebraccatus egg mortality at two ponds in Panama. (a) Total egg mortality increased in clutches not rained on during the first 24 h after oviposition (dark bars) at Bridge Pond but not at the more heavily shaded Ocelot Pond, where mortality was similar if eggs were rained on (light bars) or not during this period (generalized linear model, F1,346 = 0·8, P = 0·38, pond, F1,346 = 66·4, P < 0·0001, rain × pond, F1,346 = 5·2, P = 0·024). (b) Eggs not rained during the first 48 h had higher mortality at both ponds, due mainly to increased desiccation and ant and wasp predation, compared to clutches that received rain during that period (F1,346 = 11·7, P = 0·0007, pond, F1,346 = 68·3, P < 0·0001, rain × pond, F1,346 = 12·2, P = 0·0005). Asterisks indicate significantly different egg mortality. N24 hours: Bridge Pond – No rain = 70 clutches, Rain = 114 clutches; Ocelot Pond – No rain = 70 clutches, Rain = 96 clutches. N48 hours: Bridge Pond – No rain = 49 clutches, Rain = 135 clutches, Ocelot Pond – No rain = 40 clutches, Rain = 126 clutches. Data are mean + SE.
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Before wasp predation trials, hydrated clutch mass had increased 330 ± 74% due to water absorption, and dehydrated clutches had lost 62 ± 3% of their original mass to evaporation. These amounts of hydration and dehydration correspond to the extremes of measured clutch thicknesses (Fig. 2a). Clutch hydration clearly affected wasp–egg interactions. Although hydrated and dehydrated clutches were positioned side by side, wasps visited dehydrated clutches more often than hydrated clutches (24·7 ± 5·7 vs. 12·0 ± 3·7 total visits per clutch, respectively; paired t-test, t9 = −3·21, P = 0·01). Wasps spent significantly more time feeding and exploring on dehydrated clutches than on hydrated ones (26·2 ± 4·3 vs. 3·4 ± 1·4 min, respectively; paired t-test, t9 = −5·41, P = 0·0004). Most importantly, wasps killed over seven times more embryos from desiccated clutches than from hydrated clutches (Fig. 4a; GLM, treatment, F1,18 = 87·629, P < 0·00001). Some embryos were killed and left in the clutch, some were eaten, and others were carried away, presumably to the wasp's nest. Neither age of the eggs nor clutch position on the brick (left or right) affected predation, and so these factors were excluded from the final model (GLM; age, F1,16 = 0·36, P = 0·55; side, F1,16 = 0·22, P = 0·65).
Figure 4. Differential predation by ants and wasps on dehydrated (dark bars) and hydrated (light bars) clutches of Dendropsophus ebraccatus. (a) The proportion of eggs killed by social wasps (Polybia rejecta and Agelaia centralis) foraging on dehydrated and hydrated clutches in paired choice tests (generalized linear model, F1,18 = 87·629, P < 0·0001). Trials were stopped when mortality reached 50% in one clutch. (b) The proportion of eggs eaten by ants (Azteca sp.) from dehydrated and hydrated clutches in paired choice tests (F1,20 = 33·684, P < 0·0001). (c) The predation rate (number of eggs eaten per hour) on dehydrated and hydrated clutches exposed to ants during no-choice tests (paired t-test, t4 = −15·22, P = 0·0001). Nwasp choice = 10, Nant choice = 11, Nant no-choice = 5 clutches per condition. Data are mean + SE.
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Clutches exposed to Azteca sp. ants varied in similar ways. Hydrated clutches had gained 407 ± 33% of their original mass in water, while dehydrated clutches had lost 58 ± 2% of their mass. Ants consumed 7·4 times more eggs from desiccated clutches than from hydrated clutches (Fig. 4b; GLM, F1,20 = 33·684, P < 0·0001). During predation choice trials, we observed more ants foraging on dehydrated clutches (15 ± 3 ants per clutch) than on hydrated clutches, where we never observed ants trying to eat eggs (paired t-test, t10 = 4·98, P = 0·0005). Although we did not see predation of hydrated eggs during our hourly observations, a small number were consumed during trials; we attribute this to ants since we saw no sign of other predators on these clutches. Ant predation was similar at both ponds where trials were conducted, and ants killed more 2-day-old eggs than 1-day-old eggs (GLM, pond, F1,19 = 0·55, P = 0·47; age, F1,18 = 6·9, P = 0·02).
In no-choice tests ants also preyed on dehydrated clutches more than hydrated ones. All dehydrated eggs were eaten while only 52 ± 8 % of hydrated eggs were consumed, despite being exposed to ants for longer (GLM, F1,8 = 75·99, P < 0·0001). All dehydrated egg trials ended when all eggs were eaten, whereas all hydrated egg trials ended at nightfall. In addition, ants consumed dehydrated eggs three times faster than hydrated ones (Fig. 4c; paired t-test, t4=−15·22, P = 0·0001).