Hunting often devastates populations of large mammals, and this may have impact on other animal and plant communities. In two recent studies (Effiom et al. 2013; Effiom et al. 2014) we assessed this impact in African tropical forests. We compared sites of hunted and protected rainforests in Cross River State, Nigeria, with respect to community composition of primates, other mammals, birds, plant seedlings, and mature trees.

In hunted sites populations of important seed dispersers - including the Cross River gorilla, Gorilla gorilla diehli - were drastically reduced while seed predatory mammals increased in abundance. However, the community composition of birds was similar in both types of forests. In protected forests seedlings of primate-dispersed plant species dominated, whereas in hunted forests the seedling community was shifted towards one dominated by abiotically dispersed species.

The change in the seedling composition was probably both a consequence of reduced seed dispersal by primates, and increased seed predation by e.g. rodents. The results predict a rarity of primate-dispersed trees in future tropical forest canopies - a forest less diverse in timber and non-timber resources. In recent decades, it has become clear that hunting is a severe threat to primate populations alongside habitat destruction. Increased hunting is caused by increased demand for meat due to growing human populations in the tropics, and improved infrastructure, partly as a consequence of logging in remote forest areas (Peres & Lake 2003). Better roads facilitate the transportation of hunted animals from the forest to urban consumers.

Large primates are among the largest frugivores in African forests, and play a significant ecological role through primary seed dispersal. They are particularly important dispersers of large-seeded plants and may be the sole dispersers of some tropical plant species. This means that seed dispersal and subsequent recruitment of many plant species may be severely disrupted without the large primates. Our aim therefore was to quantify the effect of hunting on community composition of mammals, plant seedlings and birds. Secondly we wanted to know if the dispersal role of primates will be compensated by other frugivores, such as large frugivorous birds and rodents.

We established study sites in three different areas (Okwangwo division of the Cross River National Park, Mbe Mountain Community Wildlife Sanctuary, and Afi Mountain Wildlife Sanctuary) within a large more or less continuous evergreen forest expanse in southeastern Nigeria (6° 10' N, 9° 0' E). Within each area we identified one study site that was relatively well protected from hunting and one that was not, and could thus make comparisons between the sites within each pair. These forests have high primate endemism including the most range restricted, critically endangered Cross River gorilla, and the newly recognized Nigerian-Cameroon chimpanzee, Pan troglodytes ellioti.

From 2009 to 2011 we made diurnal mammal and bird counts, and surveyed the mature trees along 4 km transects in each site, and the plant seedlings (≤1 m tall) in 12 plots of 5 x 5 m in each of the six sites. In total we observed three species of large primates (gorilla, chimpanzee, and drill, Mandrillus leucophaeus), and three species of smaller monkeys (putty-nosed monkey, Cercopithecus nictitans, Mona monkey, C. mona, and red-eared monkey, C. erythrotis). We also observed a number of other mammals, including rodents (squirrels, Anomalurus spp.; brush-tailed porcupine, Atherurus africanus; cane rat, Thryonomys swinderianus; giant rat, Cricetomys spp.) and ungulates (blue duiker, Philantomba monticola; red and yellow-backed duikers, Cephalophus spp.; red river hog, Potamochoerus porcus; rock hyrax, Procavia capensis ruficeps). A total of 131 bird species were recorded during surveys. We found 113 species of mature trees and species of 83 plant seedlings in the whole survey.

Our analyses showed that there were striking differences in the mammal and seedling communities between hunted and protected sites. In the hunted sites both large and small primates were strongly reduced. We observed three times as many groups of large primates and twice as many groups of small primates in protected forests, compared to the forest sites where hunting took place. The effects on the other mammals were also striking: we observed 14 times as many (groups of) rodents and twice as many groups of ungulates in the hunted forests. Thus, hunting clearly and dramatically shifts the mammal community from one where primates are common and important to one dominated by large rodents. Primates are probably the most preferred game, and they are known to be very sensitive to hunting, so their disappearance comes as no surprise. However, the higher abundance of the large rodents and the ungulates is perhaps more surprising, as many of these species are themselves being hunted.

Unlike the rodents, the species composition of birds, which are rarely hunted in this area, was not different between hunted and protected sites. That is, not even the large frugivorous birds, such as hornbills or turacos, responded to the change in primate abundance between sites, even though primates and these birds often exploit similar food resources.

Importantly, we found that the seedling community was radically changed in hunted sites. In the protected sites, the most commonly represented species on the forest floor are those with large fruits and seeds, which are eaten and dispersed by primates. Less common are species with other dispersal modes, i.e. dispersed vegetatively, by wind, or other abiotic means (hereafter abiotic dispersal), or by birds or other non-primate animals. That is, the species composition of the seedlings in the protected sites is similar to the composition among the mature trees in the forests, which was the same in hunted as in protected sites. However, in the hunted sites the forest floor looked quite different. There, the species dispersed by other animals and by abiotic means were dominating, and primate dispersed species were in a minority.

We conclude that the difference in the seedling layer is caused primarily by the restricted seed dispersal of primate-dispersed species due to the paucity of large mammalian seed dispersers in the hunted sites, possibly in combination with the increase of large rodent seed predators in hunted sites. This conclusion concurs with the predictions generated by the Janzen-Connell model (Janzen 1970; Connell 1971). That model predicts that without effective dispersal agents most animal-dispersed plants will experience depressed recruitment as their seeds will mostly be clumped beneath parents where they are easily attacked by predators. Thus, in the protected forests where primates are still relatively abundant, large seeded primate-dispersed species are the most common and dominant among the seedlings, just as they are among mature trees. The opposite is the case in hunted forests, and the small, abiotically dispersed seeds are more evenly dispersed on the hunted forest floor and seem to escape predation to a greater extent.

Among the tree species, we can identify a number of winners and losers from hunting. Only 33 species appear to be winning from hunting (of which 33% were primate dispersed whereas 42% were abiotically dispersed), while 48 species are losers (of these, 65% were primate dispersed and 15% abiotically dispersed).

Our study highlights that key seed dispersal agents, as well as the primate-dispersed tree species, may become severely reduced even without direct effects of logging or other anthropogenic disturbances if the bushmeat crisis persists. Such loss of tree species would result in a less diverse range of food and fiber resources for both animal and human populations.

Lastly our results show that community composition of frugivorous birds was practically unaffected by hunting and the resulting lower abundances of primates. This also concurs with the conclusions of Poulsen et al. (2002) that the quantitative dietary overlap between primates and birds is rather small in forests with intact primate populations. Therefore at the moment it does not appear that the remaining dispersing animals (birds or mammals) compensate for the loss of primates and their effective seed dispersal role. That is, there is no indication that primates are redundant in this forest ecosystem.

Edu O. Effiom and Ola Olsson

References

Connell, J. H. (1971): On the role of natural enemies in preventing competitive exclusion in some marine animals and in rain forests trees. In: Dynamics of populations (eds. P. J. den Boer & G. R. Gradwell), pp. 298-312. Wageningen, The Netherlands (Centre for Agricultural Publications and Documentation)

Effiom, E. O. et al. (2013): Bushmeat hunting changes regeneration of African rainforests. Proceedings of the Royal Society B 280, no. 1759, 20130246

Effiom, E. O. et al. (2014): Changes of community composition at multiple trophic level due to hunting in Nigerian tropical forests. Ecography 37, 001-011, doi: 10.1111/j.1600-0587.2013.00359.x

Janzen, D. H. (1970): Herbivores and the number of tree species in tropical forests. American Naturalist 104, 501-528

Peres, C. A. & Lake, I. R. (2003): Extent of nontimber resource extraction in tropical forests: Accessibility to game vertebrates by hunters in the Amazon basin. Conservation Biology 17, 521-535

Poulsen, J. R. et al. (2002): Differential resource use by primates and hornbills: Implications for seed dispersal. Ecology 83, 228-240