Overhunting of mammals may negatively affect plant populations though indirect impacts on mammal-plant interactions such as herbivory. In this paper, we examined how hunting of terrestrial mammals impacts the survival of seedlings and juveniles of the palm Astrocaryum gratum. To determine A. gratum seedling survivorship patterns, an experiment with seedlings in 25 × 250-m plots exclosures and different levels of mammal species presence was conducted: all mammals, only Tayassu peccari potentially a major seedling predator and no animals excluded. More than 50,600 non-adults were measured for 27 months. We replicated these treatments in three forest categories: 1) no hunting, with an intact mammal community, 2) a lightly hunted region and 3) a heavily hunted area. Seedling survivorship under natural non-experimental conditions was highest in the heavily hunted (S(T) = 0.72), lower in moderate and lowest in unhunted forests. Experiments revealed that T. peccari was the main agent of palm seedling mortality and the most important factor determining seedling and juvenile survivorship, for example they caused the 84.61% deaths of the seedlings in unhunted forests. Thus, T. peccari feeding habits can influence forest dynamics and forest structure. T. peccari was also susceptible to hunting pressure and as the main seed and seedling predator in the system, its extinction should affect the survivorship and distribution of A. gratum in forests.
The overhunting of animals can impact plant species abundance and diversity through linked ecological processes in tropical forests (Aliaga-Rossel, 2011 [
Dirzo and Miranda, 1999 [
White-lipped peccary (WLP; Tayassu pecari) and the Chonta palm Astrocaryum gratum are ecologically important species (Aliaga-Rossel, 2011 [
Here, we use WLP and Chonta palm as model to understand the effect of removing or reducing populations of a potential keystone vertebrate consumer of seedlings versus all vertebrate species. First, using a natural experimental approach, we compare seedling survivorship in three types of forests with high, low and no hunting pressure, testing the conflicting predictions of most defaunation studies that vertebrate species can increase or decrease seedling mortality. We first test the hypotheses under conditions of complete and partial extirpation or normal levels of vertebrate species using an observational approach and a natural experiment. We also tested the hypotheses experimentally by controlling access to planted seedlings in plots (exclosures) in examples of the three forest types. In the natural experiment, we predicted that adult and seedling densities of A. gratum would be lowest in unhunted forests and highest in areas where all vertebrate herbivores (e.g. agouti Dasyprocta punctata, peccary Tayassu peccary, tapir Tapirus terrestris) have been reduced or extirpated. To tease apart the effect of all vertebrates present versus only the WLP, we predicted that experimental treatments would follow the patterns observed naturally in the three forest types: 1) allowing access to treatments by all mammals (Control) would result in the lowest seedling survivorship and recruitment levels. 2) Exclosures simulating total defaunation would show the highest palm survivorship. 3) We expected no difference in seedling survivorship between peccary-exclusion treatments in all forest types and the control situation of all vertebrates excluded. We also predicted that all effects would remain constant in the three forest types.
The study was conducted in two areas of lowland forest in Bolivia, the Madidi National Park, and Natural Area of Integrated Management (13˚20' S - 14˚00'S, 68˚10' W - 69˚10'W), and Pilón Lajas Biosphere Reserve and Indigenous Territory (14˚25' S - 15˚27'S, 66˚55' W - 67˚40'W). These adjacent areas share comparable landscapes and altitudes (altitude range = 200 - 6000 masl) and support similar ecosystems and species (Aliaga-Rossel, 2011 [
Three forest types with similar vegetation experiencing different levels of hunting pressure and therefore different mammal density were selected for study (Aliaga-Rossel, 2011 [
The unhunted area was located inside Madidi National Park, where terrestrial mammal communities remain intact (Perez, 2008 [
Following Antonik, 2005 [
For survivorship analysis, we divided A. gratum into five growth categories: Seedling includes plants up to 50 cm in height, and individuals with emerging plumules or with two bifid euphylls. This size range equals seedlings up to about two years old (Aliaga-Rossel, 2011 [
The density of Astrocaryum was the number of individual plants present in the determined area. The number of adult A. gratum capable of producing flowers and fruits was also noted along the 250 × 2-m transect. All sub-adult A. gratum within each transect were also recorded and checked monthly, with their condition recorded as alive or dead.
If dead, the cause of mortality was determined based on physical evidence and animal sign and classified as: 1) Insect attack: usually caused by different caterpillar species or leaf cutter ants. Species’ sign consisted of furrows left on the leaves or small holes on the leaf surface; 2) White-lipped peccary: seedlings uprooted and root base bitten off, unmistakable hoof tracks and/or characteristic soil removal and rooting; 3) Other vertebrate: mainly deer as determined by the presence of tracks, or sign of herbivory on leaves; 4) Fungus and other microbial pathogens: either a hole in the leaf epidermis, or fungus growing through stomata. Spores of some fungi attack leaves, creating dead spots or killing the whole leaf; 5) Unknown: the agent of mortality could not be determined, for example, indeterminate causes of desiccation (seedling standing but completely dried).
The non-parametric Kaplan-Meier survival estimator S [T] (Kaplan and Maier, 1958 [
To determine the effect of vertebrate seedling predators on the survivorship and recruitment of A. gratum. We used a randomized block design to quantify the effects of seedling consumption by vertebrates. Treatments consisted of experimental plots where: 1) all vertebrates were excluded (total fenced-exclosure), 2) only WLP were excluded (peccary fenced-exclosure), or 3) no species were excluded (no fencing around plot). A block sample consisted of each of the three treatments spaced 1 - 5 m apart. Three blocks (nine treatments), each separated by 50 - 75 m formed a plot. A total of 12 blocks where located in each forest type.
The all-vertebrate (total) exclosure consisted of a 1 × 1-m soil area enclosed by a galvanized wire mesh fence (50 cm high, <1 cm2 mesh size). The wire mesh was fixed to vertical wooden poles at the corners and staked to the soil to prevent mammals from pushing underneath. The top of the structure was covered with the same wire material to complete enclosure. All contact points between mesh and stakes were secured tightly with wire. A test run of the exclosure at the beginning of the study, indicated that leaves accumulating on top of the mesh might reduce sunlight and affect seedling growth. Thus, leaves and debris were removed each month from the top of all total exclosures.
The peccary exclosure consisted of the same galvanized wire fencing but mesh size was 2 cm2. Fencing began at 15 to 20 cm above the ground and reached a 50 cm height. Wooden poles running parallel to the ground at a 15 cm height served to secure the wire mesh. This design prevented peccaries (white-lipped peccaries and potentially collared peccaries) from rooting into the sides of the treatment but allowed smaller vertebrates such as rodents to pass beneath and through the mesh. There was no covering mesh on this exclosure type, allowing larger mammals such as deer, tapir, and birds access over the fencing. Peccary head and neck morphology did not enable them to reach into exclosures, similar to Antonik, 2005 [
The open or control treatment consisted of an unfenced area marked with 5 - 10 cm long wooden poles placed at the four usual corners as the exclosures. This treatment allowed access for all animals. Soil was cleaned around the treatment to facilitate the identification of the tracks of any terrestrial vertebrate visiting the site.
Each experimental treatment (total, WLP and open) contained 16 seedlings, planted in four rows of four with at least 20 cm between rows. Seedlings planted in the treatments were collected opportunistically from beneath different adult trees from distant unstudied areas. Only seedlings in good condition, with an emerged plumule and endocarp still attached were collected for experiments. The proportion of open canopy above each sample was measured using a spherical crown densiometer to ensure similar light conditions for each treatment.
Treatments were set out in November to December 2008 and monitored monthly until January 2011 (25 mo). Survivorship of seedlings was recorded at each visit and causes of mortality noted. Notably, the exclosures were designed to restrict vertebrate predation, and all other sources of seedling mortality, such as fungal attack, were assumed to be constant among plot type treatments.
A factorial ANOVA was conducted to determine if statistical differences in seedling survivorship were present among treatments and forest types with the plots and treatments also included, and to determine the effects of the exclosures in the forest a simple ANOVA was used. The survival rate (σ) of seedlings was derived for each forest category (unhunted, moderately hunted and hunted) and treatment for those that survived to each recording event (s) divided by the number of live plants identified at the start of the study (N) Thus, σ = s/N. The probability for moving from seedlings growth stage to the next was obtained by considering the number of plants reaching the next size class after 1 y: γ = r/s.
Mean adult palm densities differed amongst the three forest types, with the unhunted forest supporting mean ± SD 19.6 ± 12.50 indiv∙ha−1 (n = 49), the moderately hunted with 21.6 (n = 54, SD = 4.65) and the hunted one with 46 indivi∙ha−1 (n = 115, SD = 19.20). Average densities for seedlings, seedling 1, juveniles and saplings were all significantly different amongst the three types of forest, with the hunted and moderately hunted forest supporting higher seedling densities relative to the unhunted sites. The greatest difference was between forests with heavy hunting pressure relative to the others. There was little difference between forests with no-hunting and moderate hunting. A positive relationship occurred between adult and seedling density in all forests (PTE R2 = 0.6, p = 0.043). Areas with high adult density had higher seedling densities.
More than 50,600 non-adult A. gratum were recorded and monitored in three types of forests. An average of 513 individuals (SD = 60) occurred in unhunted, 685.2 (SD = 48.98) in moderately hunted and 1455 in hunted forest at the end of the study (
Seedling survivorship in all size classes was significantly different amongst the three forest classes (F2,9 = 16.4; p < 0.001), with the lowest occurring in unhunted (S(T) = 0.39, 95% C.I. ±0.03), followed by moderately hunted (S(T) = 0.66, 95% C.I. ±0.03) and lastly the heavily hunted forest (S(T) = 0.72, 95% C.I. ±0.02) (
The estimator used independently for seedlings indicates a significant difference in the survivorship rates of the three types of forest (F2,9 = 22.34; p < 0.0001); with the lowest seedling survivorship in the unhunted (S(t) = 0.255, 95% C.I. ±0.02); followed by the moderately hunted (S(t) = 0.58, 95% C.I. ±0.034) and then the hunted forest (S(t) = 0.672, 95% C.I. ±0.03 (
From January 2009 to January 2011, 576 seedlings of A. gratum were followed in the three experimental treatments. We observed different degrees of seedling survivorship amongst treatments with a significant interaction between exclosure type and forest, as well as significant main effects of both forest and exclosure type (
In contrast, seedling survival in the control plots differed significantly amongst the three forest types (control exclosure: Forest F2,9 = 164.56; p < 0.0005), with the highest mortality recorded during the first three months of the study. In the
Source | DF | Seq SS | Adj SS | Adj MS | F | P |
---|---|---|---|---|---|---|
Forest | 2 | 195.019 | 195.019 | 97.509 | 54.72 | 0.000 |
Plot (Forest) | 9 | 25.278 | 25.278 | 2.809 | 0.68 | 0.715 |
Block (Forest Patch) | 24 | 98.444 | 98.444 | 4.102 | 1.52 | 0.092 |
Exclosure | 2 | 602.074 | 602.074 | 301.037 | 111.76 | 0.000 |
Forest* Exclosure | 4 | 554.62 | 554.62 | 138.66 | 9.78 | 0.000 |
Error | 66 | 177.778 | 177.778 | 2.694 | ||
Total | 107 | 1429.407 |
first month for the controls, the unhunted forest presented a survivorship of 60.93%, the moderately hunted forest 89.06%, and the heavily hunted forest 91.66%. During the second month, seedling survivorship fell by half, dropping to 87.5% and 89.1% for the moderately and heavily hunted forest, respectively. After a year, survivorship fell to 20.8% in the unhunted, 55.21% in the moderately hunted and 69.3% for the hunted forest. After two years survivorship dropped 5.02% in the unhunted, 49.4% in the moderately and 59.89% for the heavily hunted forest (
We were unable to identify the main cause of mortality in total exclosures for all forest types (81.25% for unhunted forest, 87.75% in the moderately hunted and 99.23% for the heavily hunted forest). The next most important agent of mortality was fungus and insect infection (less than 20%) (
In only one case did peccaries impact seedlings in a peccary exclosure, when three (3.3% of the total) were dug up by white-lipped peccaries in the unhunted forest. Sign remnants indicated that rodents and other mammals did enter these exclosures. We registered only two events of mammal herbivory on seedlings inside these, both in the unhunted forest. In both instances a deer (Mazama sp.) foraged over the fence and consumed a few leaves but the seedling survived. In month six, a single seedling death was caused by an insect eating the apical meristem. A higher number of attacks by insects were detected in the moderately and hunted forest compared to the unhunted forest (
In the control plots, the highest seedling mortality (
A few seedlings were killed by falling trees and branches in two exclosures and, but most experiencing such events survived until the end of the experiment (
this rarely translated into death. There was some insect attack on several seedlings, but the first death caused by insects (herbivory by caterpillars) was registered only in the heavily hunted forest (in the peccary exclosure) in the third
Exclosure | Insect | Mammals | Peccary | Fungus | Unknown | |
---|---|---|---|---|---|---|
Unhunted | All | 6.25 (3) | 0 | 0 | 12.50 (6) | 81.25 (39) |
Peccary | 5.50 (5) | 2.19 (2) | 3.29 (3) | 4.39 (4) | 84.61 (77) | |
Control | 2.74 (5) | 1.09 (2) | 84.6 (154) | 2.74 (5) | 8.79 (16) | |
Moderately | All | 2.04 (1) | 0 | 0 | 10.2 (5) | 87.75 (43) |
Peccary | 3.44 (3) | 0 | 0 | 8.05 (7) | 88.5 (77) | |
Control | 8.4 (8) | 10.5 (10) | 1.05 (1) | 7.37 (7) | 72.63 (69) | |
Hunted | All | 1.96 (1) | 0 | 0 | 9.80 (5) | 88.24 (45) |
Peccary | 2.50 (2) | 0 | 0 | 8.86 (7) | 88.61 (70) | |
Control | 3.89 (3) | 2.60 (2) | 0 | 10.39 (8) | 83.11 (64) |
survey month. Unknown causes accounted for 8.0%, 72.6% and 83.1% of mortality (including desiccation) in unhunted, moderately and the heavily hunted forest respectively.
As Astrocaryum gratum was evaluated in having aggregated patterns in seedlings and juvenile stages in natural stands (Choo, et al., 2017 [
White-lipped peccaries were responsible for seeds, and most of the Seedling mortality in unhunted forest sites (Aliaga-Rossel and Fragoso, 2017 [
We did not found evidence of deaths caused by vertebrates in the juvenile age class. For this class, most deaths were due to tree falls or causes we could not identify. Saplings had the highest survival rate in all three forest types (survivorship higher than 90%), possibly because (as mentioned above) herbivore species prefer seedlings and softer plants (Krebs, 2001 [
In the moderately hunted forest, small groups of 5 to 10 WLP remained. In this forest, we only registered one seedling death, when WLP rooted in a control plot. In comparison, the unhunted forest supported a high density of WLP (and other mammals), and groups of up to 300 WLP disturbed and turned over litter and soil layers within A. gratum areas. Here, they killed 65 percent of seedlings within 5 months of their sprouting, mainly uprooted seedlings to eat attached endocarps. Other vertebrates or agents did not generate significant mortality. In contrast, the moderately hunted forest supported very few WLPs and as predicted few seedlings (only one) were killed in control plots. No WLPs were observed in the hunted forest and no seedlings were killed by the species there. Deaths were attributed to unknown causes, such as pathogens, larvae, and rodents. These results support the WLP-plant dynamics observed with other plant species elsewhere, where defaunation results in higher seedling densities (Fragoso, 2005 [
Our experimental and observational results thus indicate that WLP are key agents of seedling death and potentially can create significant changes in tropical forest structure as suggested by others (Antonik, 2005 [
Seedling mortality in the open control treatment was higher than at the other exclosure types and followed the pattern observed naturally on the transects. Seedling mortality during the first four months in the controls was similar amongst unhunted and mildly hunted forests (75% and 79%, respectively). This similarity can be attributed to agoutis uprooting seedlings to consume the attached endosperms in the latter area compensating for the lack of death due to WLP. Total exclosures recreated a situation of a forest with only invertebrate predators; this treatment maintained similar numbers of seedlings across the three forest types. As white -lipped peccaries where the main agent of seedling mortality where they are present in normal densities, their exclusion from these plots, probably explain why seedlings here experienced nearly complete survival in all forest classes.
Research on the effects on seedling mortality caused by vertebrates or invertebrates has shown varying results in different studies (e.g., Beck et al., 2013 [
White-lipped peccary populations may fluctuate greatly over decades perhaps because of outbreaks of disease (Fragoso, 2005 [
Thanks to the Russel Train education program (WWF), to International Foundation for Science (IFS), and WCS—Bolivia. Thanks also to Robert Wallace. Idea Wild provided key equipment. Thanks to the National Service of Protected Areas (SERNAP), to the Asuncion del Quiquibey, Tsimane-Moseten indigenous community and to Heydi Montecinos for her field assistantship, and all the local field guides of the community. Thanks to David Duffy, Christopher Lepczyk, Andrew Taylor, Tamara Ticktin, Tom Ranker, and Donald Drake. Thanks to Stephan Beck and the National Herbarium of Bolivia. Thanks to Kirsten Silvius for her initial collaboration. Thanks also to Mark Gregory, Paula Capece, Daniel Hagaman for manuscript reviews.
The authors declare no conflicts of interest regarding the publication of this paper.
Aliaga-Rossel, E., Fragoso, J.M.V. and Moraes R., M. (2022) Defaunation Increases the Survivorship of the Palm Astrocaryum gratum in a Submontane Tropical Forest. Open Journal of Ecology, 12, 306-323. https://doi.org/10.4236/oje.2022.125018