Phenology of Predation on Insects in a Tropical Forest: Temporal Variation in Attack
Rate on Dummy Caterpillars
Freerk Molleman1,2,6*, Triinu Remmel1,3, and Katerina Sam4,5
1
Institute of Ecology and Earth Sciences, University of Tartu, Vanemuise 46, EE-51014, Tartu, Estonia
2Universite de Rennes 1, ECOBIO, Campus de Beaulieu, 35042, Rennes, France
3Department of Plant Physiology, Estonian University of Life Sciences, Fr. R. Kreutzwaldi 5, 51014, Tartu, Estonia 4
Biology Centre CAS, Institute of Entomology, Branisovska 31, CZ-370 05, Ceske Budejovice, Czech Republic
5
Faculty of Science, University of South Bohemia, Branisovska 1760, CZ-370 05, Ceske Budejovice, Czech Republic
ABSTRACT
In communities of tropical insects, adult abundance tends to fluctuate widely, perhaps in part owing to predator–prey dynamics. Yet, temporal patterns of attack rates in tropical forest habitats have not been studied systematically; the identity of predators of insects in tropical forests is poorly known; and their responses to temporal variation in prey abundance have rarely been explored. We recorded incidence and shape of marks of attacks on dummy caterpillars (proxy of predation rate) in a sub-montane tropical forest in Uganda during a yearlong experiment, and explored correlations with inferred caterpillar abundance. Applying the highest and lowest observed daily attack rates on clay dummies over a realistic duration of the larval stage of butterflies, indicates that the temporal variation in attack rate could cause more than 10-fold temporal variation in caterpillar survival. Inferred predators were almost exclusively invertebrates, and beak marks of birds were very scarce. Attack rates by wasps varied more over time than those of ants. Attack rates on dummies peaked during the two wet seasons, and appeared congruent with inferred peaks in caterpillar density. This suggests (1) a functional response (predators shifting to more abundant resource) or adaptive timed phenology (predators timing activity or breeding to coincide with seasonal peaks in prey abundance) of predators, rather than a numerical response (predator populations increasing following peaks in prey abundance); and (2) that predation would dampen abundancefluctuations of tropical Lepidoptera communities.
Key words: artificial prey; development time; functional response; Lepidoptera; population dynamics; seasonality; sentinel caterpillar; Uganda.
LOW MAGNITUDE OF SEASONAL CLIMATIC VARIATION IN MUCH OF THE TROPICS COULD CAUSE NATURAL ENEMIES SUCH AS PREDATORSto have a relatively large effect on abundance fluctuations in tropical insect communities. However, there have been only a few studies addressing temporal variation in predation rate in tropical habi-tats. In Panama, attack rates on clay dummies were higher during a wet season than during a dry season (Richards & Coley 2007). However, some studies on predator abundance did not reveal sig-nificant seasonal fluctuations (e.g., birds in Panama—Karr 1976, bats in Panama—Wilson 1971, various predatory insects in tropi-cal Australia—Frith & Frith 1985). To our knowledge, no studies on the attack rates on insects (and artificial insects) for a tropical habitat has been published that span a whole year or longer.
While there is little direct evidence on the role of predation in determining community dynamics in tropical insect communi-ties, natural enemies appear to play an important role. Several studies have provided evidence that tropical herbivorous insects undergo seasonal changes in abundance and that this is correlated
with precipitation patterns (e.g., Wolda 1978a, Silva et al. 2011, Valtonen et al. 2013, Grøtan et al. 2014). This relationship appears in part mediated via vegetation growth: timing of peaks in butterfly abundance tracks variation in timing of peaks in vege-tation greenness (Valtonen et al. 2013). Thus, folivorous insects appear to take advantage of new leaves that are more abundant during rainy seasons (Richards & Windsor 2007). However, rain-fall tends to only explain a small proportion of variation in tropi-cal butterfly abundance and community composition (Grøtan et al. 2012, 2014, Valtonen et al. 2013), suggesting a particularly important role of natural enemies in driving tropical insect popu-lation dynamics. Similarly, Morais et al. (1999) argued that natural enemies play an important role in shaping caterpillar abundance patterns in a dry tropical environment. This may corroborate the trend that interactions among species are more intense in the tropics (e.g., stronger density dependence; Schemske et al. 2009).
Population dynamics resulting from predator–prey interac-tions may vary widely in pattern. For example, following an increase in prey numbers, the abundance of predators, and there-fore predation rates, may increase as a result of higher reproduc-tive rates in the predator population (Lotka 1910, Volterra 1931). This increase in predator abundance would occur after a delay, thus causing prey populations tofluctuate. Alternatively, predation
Received 30 September 2014; revision accepted 9 June 2015.
6Corresponding author; e-mail: [email protected]
*Current address: Vanasiri Evolutionary Ecology Group, School of Biology, Indian Institute of Science Education and Research, Thiruvananthapuram, Kerala, India
rates may increase more immediately, when existing predators switch their diet to utilize the more abundant resource (Func-tional Response: Holling 1959a,b), which would dampen prey abundance fluctuations and promote synchrony among species (Korpimaki et al. 2005, Wang & Loreau 2014). Moreover, preda-tors may be selected to time their phenology to seasonal peaks in prey abundance (adaptive phenology: Both et al. 2009), which would also dampen prey population fluctuations. Therefore, information on temporal variation in attack rates, and the rela-tionship between prey abundance and attack rate, can provide insight into the dominant types of predator–prey dynamics (Ber-ryman 1999). However, such information is scarce for tropical insect communities. Studies of vertebrate predators of tropical insects have shown that hunting activity and reproduction attempts coincide with seasonal peaks in insect abundance (Lister & Aguayo 1992, Wikelski et al. 2000). In addition, some tropical studies suggest that peaks in abundance of invertebrate predators coincide seasonally with those of their prey (e.g., mantis in Panama—Wolda 1978a, web making spiders in Panama—Robin-son & RobinPanama—Robin-son 1970). However, no study in a tropical forest has directly (or via proxies other than ‘season’) related attack rates with insect prey abundance.
The duration of delays of numerical responses of predators depends on the development time of predators, and the strength of functional responses depends on alternative foods of predators (e.g., Walker & Jones 2001, Lewinsohn et al. 2005, Richards & Coley 2007). Therefore, information on predator identity would contribute toward understanding the effect of predators on abun-dancefluctuations of their prey, because different types of natural enemies have different development times and tend to have dif-ferent diet breadths. However, the relative contribution to cater-pillar mortality of different classes of predators is still poorly known for the tropics, and for Africa in particular (Molleman & Safian 2015). Invertebrates emerge as the dominant predators in tropical lowland forests, while birds dominate as caterpillar preda-tors in temperate sites and in tropical montane areas (Remmel et al.2011, Tvardikova & Novotny 2012, Nokelainen et al. 2014, Sam et al. 2014, Yguel et al. 2014, Ewers et al. 2015, Molleman & Safian 2015, Seifert et al. 2015, Remmel and Tammaru 2009). Non-social invertebrate predators in the tropics may show a delayed population response to their prey (Richards & Coley 2007), probably due to a numerical response to prey availability that reflects the development time of the predators. Such delays might contribute to the irregularlyfluctuating abundance of non-seasonal species, which is common in tropical herbivorous insects such as butterflies (Valtonen et al. 2013). On the other hand, gen-eralistic predators, such as ants, could respond directly to prey density (without a delay) by shifting among prey types or habitats (functional response). Therefore, information on predator identity would contribute to understanding tropical insect population fluc-tuations.
We performed a yearlong study of marks of attacks on artifi-cial caterpillars made of malleable materials (dummies; Hitchcock 2004, Howe et al. 2009, Low et al. 2014) in an African tropical forest. Our main goals were to: (1) assess the extent of temporal
variation in predation rate; and (2) to estimate the relative contri-bution of predator classes to predation on caterpillars in a tropi-cal forest. We then explored how attack rate may be related to inferred caterpillar abundance. We expected two possible scenar-ios: (1) when peaks in attack rates follow peaks in inferred cater-pillar densities with a delay, we interpret this as suggesting a population response of predators to prey density where the delay would be predator development time; and (2) when peaks in attack rates coincide with peaks in inferred caterpillar densities, we interpret this as suggesting a functional response or adaptive phenology of the predators. We discuss how predation may influ-ence the temporal dynamics of tropical insect communities.
METHODS
We conducted the study in a tropical forest near the Makerere University Biological Field Station in Kibale Forest National Park (0°33042″ N, 30°21052″ E), Western Uganda. There are two dis-tinct wet and dry seasons each year: May–August and Decem-ber–February tend to be drier than other months (Chapman et al. 2005, Stampone et al. 2011, Valtonen et al. 2013). Mean annual rainfall in the region is 1547 mm (1903–2001); mean daily mini-mum temperature is 14.9°C; and mean daily maximini-mum tempera-ture is 20.2°C (1990–2001).
We used artificial caterpillars (dummies) exposed on vegeta-tion to measure attack rates and identify predators. We used both clay and dough dummies to assess whether dummies made of different materials suggest similar temporal patterns in predation on caterpillars. Dough had been used in experiments in Estonia to offer dummies that are edible, and in that temperate system material did not affect attack rates significantly (Remmel et al. 2009). However, when more chemically oriented predators such as ants dominate, dough dummies might better reflect predation because they may be more readily attacked by chemically oriented predators, but dough dummies perhaps also incur damage from non-predacious animals. Dummies were made from modeling clay (Cernit, Number one), or dough (lard and whiteflour, 1:1) colored greenish by food coloring (Aromatic, Green 3; Table 1). These dummy types experience predation rates that are similar to actual caterpillars of the butterfly Charaxes fulvescens (dough dum-mies being more frequently damaged and clay less frequently; Sam et al. in press). Both dough and clay material were malleable, and all dummies were modeled and handled with surgical gloves. We used two sizes of dummies (2 cm and 4 cm long cylinders) with similar dimensions (Table 1).
We conducted all our trials on three common understory plant species: the shrub Allophylus dummeri Baker 1919, and sap-lings of Uvariopsis congensis Robyns & Ghesq. 1933, and Lepisanthes senegalensisLeenh., 1969 (Table 1). Each dummy was glued (Super Glue) on the central vein of a randomly selected leaf of a focal plant species at a height of ca 1.5 m, and individual dummies were placed at least 10 m apart. For each of the 20 trials (Table 1), we glued 10 individual dummies along each of 10 tran-sects that were part of the trail system and were at least 100 m from each other. On each transect, there werefive small and five
large dummies, and clay and dough dummies were alternated. While the same transects were used throughout the study, the individual plants on which dummies were glued were not the same, thus decreasing the probability that spatial memory of predators would play a role. To facilitate retrieval, the trail coordi-nates of transects were noted, and each trial the position of dum-mies at transects was labeled withflagging tape, and the distance (1–10 m) and direction (left/right) from transects noted.
Dummies were collected 3 days after their exposure (although due to bad weather, in one trial 2 days and in one trial 5 days) using scissors so that part of the leaf was taken with it. At collection, notes were taken on damages to the dummy, and presence of insects such as ants. Dummies were later carefully inspected for damages with the help of a binocular microscope at thefield station (20x). Marks were at first identified by FM (and photos taken to compare with references from elsewhere; Low et al.2014) and this skill was then transferred to three assistants who performed the damage description together (as recom-mended by Low et al. 2014), describing rather than interpreting the damage in case of doubt. These damage descriptions were later categorized by FM into distinct classes of putative predators (ants, wasps, predatory bugs, birds, rodents, other invertebrates), taking thefield notes into account. Two bugs and a mantis were observed feeding on caterpillars in the field (during a total of 3.5 years of fieldwork at the site). Video footage from the site showed nocturnal feeding on dummies by a tree-cricket, a lacew-ing, flies, and moths. Together, field observations, videos, and information from other sites (e.g., YouTube videos of orthopter-ans preying on live insects including caterpillars) demonstrate that a wide variety of predatory and non-predatory insects can be responsible for unidentified damage to dummies.
To relate attack rates on dummy caterpillars with caterpillar densities, we used two proxies of caterpillar abundance. First, we used rainfall data since timing of peaks in rainfall at this site is known to correlate with timing of peaks in adult fruit-feeding butterfly abundance 3 months later (Valtonen et al. 2013). Thus, given typical development times, the corresponding peaks in
but-terfly caterpillar abundance would have been during rainy sea-sons. Peaks in densities of herbivorous insects following peaks in precipitation, seems to be a common pattern in tropical systems, but comprehensive data are scarce (Grøtan et al. 2014). However, experience of collecting geometrid moth caterpillars at the study site (S. Holm & F. Molleman, unpubl. data) and literature (re-viewed in Valtonen et al. 2013) suggests that timing of abundance peaks of other insects tends to be similar to butterflies, so that butterflies can probably represent timing of caterpillar abundance more generally. Local rainfall was recorded daily at the study site. Long-term rainfall data (70 years) were available from the Government of Uganda meteorological records for the Station 5 in Fort Portal (ca 20 km east of the study site; Stampone et al. 2011). Average temperature varies relatively little in the study area and appears to play at most a minor role in butterfly community dynamics (Valtonen et al. 2013). Second, monthly butterfly cater-pillar abundance was estimated by the subsequent abundance of fruit-feeding butterflies (species listed in Valtonen et al. 2013, we excluded the Sevenia species that appear not to breed at the site).
To estimate the duration of exposure of individual butterfly caterpillars to predation, and the delay between larval and adult abundance of butterflies, we compiled rearing data. Eggs and caterpillars were collected in the forest, and eggs were collected from captive females. Caterpillars were reared to adulthood at the field station under ambient conditions, while noting dates of stage changes daily (egg, larva, pupa, adult). We then calculated average stage durations and egg to adult time per species. These per spe-cies averages were then averaged for all spespe-cies for which we had development-time data.
STATISTICAL ANALYSES.—Total mean daily attack rates (%), and mean daily attack rate per predator class (%), were calculated for graphic representation. The lowest, average, and highest daily attack rates on clay dummies observed were used in a demo-graphic simulation to illustrate how differences in attack rate would translate into caterpillar survival. An artificial cohort was made to suffer a constant daily predation rate for the period of a typical duration of the larval stage of fruit-feeding butterflies. By design and some accidents, the numbers of dummies in each of the treatments and trials were not equal. Unweighted means and type III sums of squares were used and compared to minimize confounding effects of unequal sample sizes (Maxwell & Delaney 2004). Dummies that went missing were excluded from analyses. As predictors of attack rate (presence or absence of damage to dummies) we tested for the main effects of type of predator (ants, wasps, predatory bugs, birds, cockroaches, small mammals, other invertebrates), type of dummy, date of exposure, size of dummy, and plant species where the dummy was exposed, and their interactions using generalized linear models (binomial distri-bution, logit link function) in Statistica 12 (StatSoft 2010). Subse-quently, Tukey post-hoc tests were performed to test for differences in attack rates between the predator classes. Date of exposure was set as a categorical factor. Temporal patterns were analyzed as cross-correlation of Time Series (Time Series/ Forecasting in Statistica 12), and lags of up to 5 months were
TABLE 1. Experimental design of predation study using dummies of either clay or dough in Kibale National Park, Uganda. Plant species: AL—Allophylus abyssinicus, LE—Lepisanthes senegalensis, UV—Uvariopsis congensis.
Dates of exposition
2010: 17, 18, 25 Mar; 2, 16, 30 Apr; 11, 30 May; 8, 25 Jun; 9 Jul; 6 Aug; 3 Sep; 1, 29 Oct; 26 Nov; 24 Dec; 2011: 21 Jan; 18 Feb;
18 Mar No. of exposed caterpillars
Type Size AL LE UV Total
Clay 2 cm 156 66 231 453
4 cm 167 91 242 500
Dough 2 cm 158 43 285 486
4 cm 143 46 308 497
inspected for the best fitting correlation. Similarly, we used cross-correlation to investigate differences in temporal patterns of the three most important classes of predators. All data were tested for normality and non-parametric tests were used when this assumption was not met.
RESULTS
Of the 1936 dummies exposed in 20 trials (Table 1), 607 showed marks of attack, yielding a mean daily attack rate of 11.6 SD 6.2%. Seven percent of all exposed dummies were lost, and were excluded from our analyses. Both date of exposure and type of dummy (clay or dough) had significant effects on attack rate, while dummy size and plant species did not have significant effects (Table 2). Daily attack rate on clay dummies ranged between 3 percent and 14 percent, averaging 6.6 percent, which would accumulate into over ten-fold differences in larval survival over months (Fig. 1). Dough dummies were attacked significantly more than clay dummies (mean daily attack rate on dough dum-mies: 16.2 SD 6.2%, Table 2), and this was the case for both ants and wasps when considered separately (Wilcoxon test, N= 20; ants: T = 39, Z = 2.25, P = 0.02, wasps: T = 16, Z = 2.25, P = 0.012). Daily attack rates on clay and dough dum-mies showed a similar temporal pattern (Fig. 2) and were signifi-cantly correlated (Table 3). Temporal variation in attacks on clay was not different from temporal variation in attacks on dough dummies (Bartlett Chi-Sqr.= 1.7, P = 0.191; clay SD = 6.2, dough SD= 9.5).
The higher proportion of dummies damaged was by ants (48.95 SD 5.3%), and then by wasps (13.8 SD 3.2%). Ant attack rate varied less over time than wasp attack rate (variance ants= 118.34 and SD = 10.8; variance wasps 129.08 and SD= 11.36; Bartlett Chi-Sqr = 5.35, P = 0.02, N = 20 trials). Other inferred damagers of dummies were too rare for further
statistical tests: predatory bugs (12 identified from damages), bee-tles (eight field notes), birds (six identified from damages), cock-roaches (three field notes), and rodents/shrews (two identified from damages). Predators could often not be identified from marks (10% of exposed and retrieved dummies), but were likely not vertebrates as these generally leave clear marks (Low et al. 2014). While ants damaged the largest proportion of damaged dummies during all trials (Fig. 3), the attack rates by predator cat-egories were not significantly correlated among periods (ant— wasp: r= 0.21; ant—unknown: r = 0.17; wasp—unknown: r = 0.04; no lag time for all).
Attack rates were highest during rainy seasons (March–May, August–November), and lowest during the June–July dry season (Fig. 2). Local rainfall during the study period correlated nearly significantly (Table 3) with mean daily rainfalls measured during 70 years (February 2011 experienced much higher daily rainfalls than usual; Fig. 2). Attack rate correlated significantly with monthly average rainfalls (measured during 70 years), but did not correlate significantly with rainfall during the exposure month (Table 3). Butterfly abundances during the study period (and hence inferred caterpillar abundance) did not correlate well with average monthly rainfalls (rainfall during the study period, rainfall measured during 70 years; Table 3). The overall attack rate on dummy caterpillars in a month correlated nearly significantly with butterfly abundances 1 month later, which corresponds with the timing of the caterpillar stage (average duration of caterpillar stage= 36 days, SD 7.0; average egg to adult time = 57 days, SD= 8.6, N = 11 species; details in Table 4). This correlation was not significant for the two dummy types separately, but both dummies made of clay and of dough had the bestfit with butter-fly abundances 1 month later (Table 3).
DISCUSSION
This first yearlong study on attack rates on (artificial) tropical insects, demonstrates temporal variation in attack rate; provides
TABLE 2. Results of generalized linear models (binomial distribution, link logit function) show that date of exposition (i.e., starting date of trial) and type of dummy had a significant effect on the probability of predation (Sample sizes in Table 1). Plant species on which dummies were exposed and size of the dummies did not have significant effects. There was an interaction between dummy type and tree species on which the dummy was exposed, where the relative attack rates on dummies on different plant species differed erratically among periods.
Waldv2 df P Date 39.792 15 0.005 Type 9.01 1 0.008 Size 3.52 1 0.088 Tree 3.81 2 0.069 Date* Type 15.86 14 0.322 Date* Size 14.48 14 0.414 Type* Size 0.32 1 0.571 Date* Tree 39.88 30 0.107 Type* Tree 6.75 2 0.034 Size* Tree 5.35 2 0.069
FIGURE 1. Survival curves of caterpillars in Kibale National Park, Uganda modeled using the daily attack rates on clay dummies during periods with minimum, maximum, and average attack rates. Attack rate was assumed con-stant with caterpillar age, as suggested by our data on two size categories.
insight into the relative contributions of predator classes to cater-pillar mortality; and suggests functional responses or adaptive phenology of predators. Although temporal variation in attack rate may seem small, and is smaller than in temperate studies
(Remmel et al. 2009), it can accumulate to over ten-fold differ-ences in the proportion of individuals that would survive the caterpillar stage, and predation can thus be expected to impact abundance fluctuations of the Lepidoptera community. During this 1 year, attack rate peaked during the two rainy seasons, when caterpillar densities were inferred to peak as well. This temporal pattern in attack rate in Uganda corroborates results from Panama, where attack rate on clay dummies was higher during a wet season than during a dry season (Richards & Coley 2007).
Long-term studies would be needed to determine if the fluc-tuation of attack rate is seasonal (reoccurring pattern). We found
FIGURE 2. Mean daily attack rate (total predation: continuous line, left Y axis) on dough (interrupted line, left Y axis) and clay (interrupted line, left Y axis) dummy caterpillars in Kibale National Park, Uganda. Attack rate is roughly congruent with mean daily rainfalls measured by a local data logger (bars, left Y axis), mean rainfall data collected during 70 years by a nearby meteorological station (bars, left Y axis) as well as inferred abundance of caterpillars (area with pattern, right Y axis). Statistical results of cross-correlation analyses are presented in Table 3. Data for whole year 2010 and beginning of year 2011 (behind interrupted vertical line) are shown.
FIGURE 3. Percentage of dummies (dough and clay taken together) dam-aged by identified classes, unknown predators, and that went missing, in Kibale National Park, Uganda.
TABLE 3. Summary of cross-correlation analyses showing for each combination the best fitting model out of the tested lag durations, (significant correlations in bold with *P < 0.05 and **P < 0.01). Dough = attack rate on dough dummies, clay= attack rate on dough dummies, total = attack rate on both types of dummies combined, local rain= monthly rainfall measured during study, average rain= average rainfall over 70 year period, butterfly abundance= abundance of butterflies in fruit-baited traps during the study period.
Basic Lagged Correlation Lag (months)
Dough Clay 0.79 0.28* 0
Local rain Dough 0.26 0.27 0
Local rain Clay 0.29 0.27 0
Local rain Total 0.27 0.27 0
Local rain Average rain 0.59 0.26* 0
Local rain Butterfly abundance 0.18 0.25 -1
Average rain Dough 0.60 0.27* 0
Average rain Clay 0.49 0.27** 0
Average rain Total 0.60 0.27* 0
Average rain Butterfly abundance 0.17 0.25 -1
Butterfly abundance Dough 0.39 0.27 1
Butterfly abundance Clay 0.33 0.29 1
that peaks in overall attack rates coincided with peaks in inferred caterpillar abundance, thus suggesting a functional response (predators switching to the more abundant resource), or adaptive phenology (predators timing activity or breeding to seasonal peaks in resources) of predators. Any relationship with caterpillar abundance needs to be tested further; preferably using caterpillar counts rather than inferences from one butterfly guild and its average response to rainfall. Butterflies contribute a minor pro-portion of the caterpillar biomass (most are moths; Heimonen et al. 2013), but it is the only group, we have (adult) temporal abundance fluctuation data on. Moreover, experiments and long-term data would be needed to assess to which extent the differ-ent predator categories have functional responses to caterpillar density, such as diet and habitat shifts, or have a seasonal adap-tive phenology selected for by predictable timing of peaks in prey abundance. To our knowledge, this has not been addressed for tropical systems. In temperate and arctic systems, adaptive phe-nology is often taken as a given and some studies aim to distin-guish between (lagged) numerical and functional responses of predators (Gilg et al. 2006, Both et al. 2009), while the one tropi-cal study on invertebrate predator prey dynamics we found is on short-lived mites, in which adaptive phenology is unlikely (Morell et al.2010). While our data do not suggest a numerical response of predators (peak in attack rate on dummies does not follow a peak in inferred abundance with a delay), the butterfly commu-nity dynamics suggest that numerical responses could be impor-tant. In particular, if predation indeed tends to coincide with peaks in caterpillar abundance, then we expect predation to dam-pen abundance fluctuations and to promote synchrony among prey species within sites (Raimondo et al. 2004, Korpimaki et al. 2005). However, populationfluctuations of insects in moist tropi-cal forests are extensive and usually lotropi-cally asynchronous among species (Wolda 1978b, Grøtan et al. 2014), including fruit-feeding butterflies at our study site (Valtonen et al. 2013). Therefore, it seems likely that lagged population responses of highly specialized
natural enemies (such as parasitoids—Smith et al. 2008, Hrcek et al.2013) also play an important role in driving abundance fluc-tuations in tropical insect communities. For example, Aiello (1992) suggested that the lag time between recovery of butterflies and their parasitoids allowed an explosion of butterflies after a severe dry season. Furthermore, environmental factors that drive tropical insect populations deserve further study, also with respect to weather effects on natural enemies (e.g., cool weather reducing predation rates by ectothermic predators).
Actual predation rates on caterpillars and the relative contri-bution of predator classes to attacks on caterpillars in the wild is partially revealed by the marks left on dummy caterpillars. Dum-mies are designed to draw attacks of visually hunting caterpillar predators such as birds and wasps, while perhaps not being rec-ognized as prey by chemically oriented predators: they are made to look but not smell or taste like caterpillars. Nevertheless, traces of feeding on dummies shows that both types of dummies are consumed by both types of predators, and will thus in part repre-sent activity of chemically oriented predators. Indeed, a large pro-portion of damage in our experiment was probably by more chemically oriented animals for which material may be important: ants and unidentified invertebrates. Therefore, dough dummies are likely to overestimate attack rates on caterpillars by attracting non-predators, while clay dummies may underestimate actual pre-dation pressure because they may be ignored by more chemically oriented predators. In particular, dough may be damaged espe-cially by ants and unknown invertebrates that would not always kill a real caterpillar (although many ant species do predate on caterpillars). Since the difference in attack rate on dough and clay dummies can differ among habitats (depending on the dominance of visual versus chemical orientation among predators), and sur-vival of real caterpillars appears to be intermediate between dough and clay dummies (Sam et al. in press), using dummies of both materials provides more insight than each in isolation. Moreover, as temporal variation in attack rates are correlated
TABLE 4. Duration of larval stage and egg to adult development time (days) for some common fruit-feeding butterfly species in Kibale National Park, Uganda.
Species Larval stage SE N Pupal stage SE N Egg-adult SE N
Bicyclus auricruda 13.0 1 50.0 6.9 1 B. mandanes 35.0 2.1 13 12.8 0.7 22 56.1 1.7 16 B. mollitia 36.0 7.5 1 14.0 1 Charaxes bipunctatus 37.0 7.5 1 16.2 1.1 5 50.0 6.9 1 C. fulvescens 38.3 0.5 223 13.8 0.3 381 59.7 0.4 314 C. numenes 52.6 1.3 31 17.3 1.3 43 78.4 1.1 36 C. pollux 44.0 3.0 6 16.0 0.6 10 63.5 2.1 11 Euphaedra alacris 29.4 1.5 25 12.9 0.9 80 51.2 1.1 38 E. eusemoides 32.7 1.8 17 8.5 1.6 38 60.5 1.6 19 E. harpalyce 33.1 2.8 7 17.7 0.3 17 58.1 2.6 7 E. medon 27.0 0.7 100 14.7 0.4 146 47.5 0.6 113 E. uganda 34.0 5.3 2 14.4 3.6 5 54.7 4.0 3 Gnophodes chelys 37.0 7.5 1 13.4 0.6 97
among clay and dough dummies in our studies, they probably can both be used separately to document temporal variation in predation pressure in tropical forests. While ants were always the most frequent attackers of dummies, different predator classes showed different temporal patterns in attack rate, so that short studies would estimate their relative contributions to attack rates on dummies imprecisely.
Attacks on dummies were mainly by social insects (ants and part of the wasps). Especially ants may be sufficiently gen-eralistic (and long-lived at the colony level) to show functional responses to caterpillar density. In addition, particular ants and wasps may have evolved a timed phenology to concentrate for-aging for caterpillars during periods when they tend to be more abundant (rainy season). However, we have little information on the phenology of ants and wasps in this tropical forest. It seems likely that ants breed throughout the year (Kaspari et al. 2001), but some species may temporally shift their foraging to different habitats on a small spatial scale (Sch€oning et al. 2008). As in the other studies in (non-montane) tropical forests, bird attacks on dummies appeared rare. In other forests, beak marks on dummies have been far more prevalent than complete removal of dummies by birds (e.g., Remmel et al. 2009), and thus nearly always complete removal of dummies by birds in our study would suppose a rather different behavior of birds toward dummies in this forest than elsewhere. Therefore, while lost dummies may be attributed to birds, we find this unlikely given the scarcity of beak marks in those dummies that were not lost.
In conclusion, we found temporal variation in predation rate on artificial caterpillars in a tropical forest that would translate into extensive variation in caterpillar survival. Attacks were mainly from invertebrates (ants, wasps, and others), while bird beak marks and damages by small mammals were very scarce. Peaks in attack rates on dummies were associated with peaks in inferred caterpillar abundance. Further studies are needed to assess sea-sonality in attack rates, and to draw more confident conclusions on relations between attack rates and caterpillar abundance, and the relative roles of numerical responses, functional responses and adaptive phenology of caterpillar predators.
ACKNOWLEDGMENTS
We thank Boniface Balyeganira, Mwesige Isaiah, Francis Katu-ramu Kanywanii, Katusabe Swaibu, and Sille Holm for their invaluable assistance in thefield and in the laboratory, and Balye-ganira Bonny and Ahabyona Peter for data entry. We are grateful to Colin Chapman for sharing climate data. We thank the Uganda Wildlife Authority (U.W.A.), Makerere University Biological Field Station (M.U.B.F.S.), and the Ugandan National Council for Science and Technology (U.N.C.S.T.) for permission to carry out the research. We are grateful to Annette Aiello and two anony-mous reviewers for insightful comments on earlier drafts of this manuscript. Funding for data collection was from the Estonian Science Foundation grants 9215, and IUT20-33, and by the European Union through the European Regional Development
Fund (Centre of Excellence FIBIR). Katerina Sam was supported by The Czech Science Foundation Grant No. 14-32024P, Triinu Remmel by the European Union through the European Social Fund’s Mobilitas postdoctoral grant (MJD161) and Institutional Research Funding (UT8-3) of the Estonian Ministry of Education and Research, and Freerk Molleman in part by a SAD grant from the Region Bretagne.
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