Insect Leaf-Chewing Damage Tracks Herbivore Richness in Modern and Ancient Forests

<div><p>The fossil record demonstrates that past climate changes and extinctions significantly affected the diversity of insect leaf-feeding damage, implying that the richness of damage types reflects that of the unsampled damage makers, and that the two are correlated through time. However, this relationship has not been quantified for living leaf-chewing insects, whose richness and mouthpart convergence have obscured their value for understanding past and present herbivore diversity. We hypothesized that the correlation of leaf-chewing damage types (DTs) and damage maker richness is directly observable in living forests. Using canopy access cranes at two lowland tropical rainforest sites in Panamá to survey 24 host-plant species, we found significant correlations between the numbers of leaf chewing insect species collected and the numbers of DTs observed to be made by the same species in feeding experiments, strongly supporting our hypothesis. Damage type richness was largely driven by insect species that make multiple DTs. Also, the rank-order abundances of DTs recorded at the Panamá sites and across a set of latest Cretaceous to middle Eocene fossil floras were highly correlated, indicating remarkable consistency of feeding-mode distributions through time. Most fossil and modern host-plant pairs displayed high similarity indices for their leaf-chewing DTs, but informative differences and trends in fossil damage composition became apparent when endophytic damage was included. Our results greatly expand the potential of insect-mediated leaf damage for interpreting insect herbivore richness and compositional heterogeneity from fossil floras and, equally promisingly, in living forests.</p></div

Pairwise host-plant similarities based on herbivores and leaf damage in living forests, and on leaf damage in fossil forests.

<p>(<i>A</i>) Inverse relations between the distributions of pairwise similarities of leaf damage (DT) and herbivore species, estimated using the Chao-Sørensen index, for host-plant species pairs at the Área Protegida de San Lorenzo (gray bars) and Parque Natural Metropolitano (hollow bars), Panamá (<a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0094950#pone.0094950.s010" target="_blank">Dataset S1</a>). Vertical axis indicates relative abundance of species pairs showing a given similarity index (horizontal axis). Similarity of DTs between host-plant pairs is much higher than similarity of herbivores, as expected from convergence. (<i>B</i>) Plant-species pairwise similarities of herbivores and leaf damage, from the Panamá crane sites (same as in <i>A</i>). (<i>C</i>) Skewed distributions of host-plant pairwise similarities of leaf-chewing damage at fossil sites (see <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0094950#s2" target="_blank">Materials and Methods</a>), estimated for (n) species at each fossil site, using the Chao-Sørensen index (<a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0094950#pone.0094950.s010" target="_blank">Dataset S1</a>). Axes are similar to those in (<i>A</i>). Yellow  =  Late Cretaceous, blue  =  Paleocene, and red  =  Eocene age. Hollow bars represent distributions of the null expectation, and numbers indicate how many host-plant species (n) and the proportion of observed pairwise estimates that fall outside the null distribution range. (<i>D</i>) Distributions of host-plant pairwise similarities of total leaf damage (i.e., including endophytic, largely specialized feeding such as mines and galls) at fossil sites as in (C), estimated as 1-Sørensen coefficient (<a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0094950#pone.0094950.s010" target="_blank">Dataset S1</a>). There is greatly increased distinctiveness in damage type composition between host plants when endophytic feeding is considered when compared to (<i>C</i>).</p

Correlations of insect and induced leaf-damage richness in two Panamanian forests.

<p>Spearman's correlations (r_s) of the number of insect species (Insect richness – IR) vs. number of leaf-chewing damage types (damage type richness – DTR) observed across 24 tropical host plant species, plotted against 1∶1 lines, include: (<i>A</i>) Total numbers of collected leaf-chewing insect species per host plant at Área Protegida de San Lorenzo (Gray, solid circles) and Parque Natural Metropolitano (black, hollow circles). (<i>B</i>) IR-DTR correlation for coleopteran species. (<i>C</i>) IR-DTR correlation for non-coleopteran species. (<i>D</i>) IR-DTR correlation after filtering out leaf damage that is unlikely to be preserved in fossil assemblages. (<i>E</i>–<i>F</i>). Separate IR-DTR correlations for insect species that induced one (monodamaging, E) or multiple (multidamaging, F) DTs when feeding. For (<i>A</i>–<i>F</i>), each data point is one host-plant species at one site; all data plot with a shallower slope than 1∶1, as expected from convergence.</p

Selected leaf-chewing insects collected from two Panamanian forests, and induced external leaf damage resulting from insect feeding experiments.

<p>(<i>A</i>) <i>Phyllophaga</i> sp. 2 (Coleoptera: Scarabaeidae) observed inducing margin feeding DT12 and DT14 on <i>Tapirira guianensis</i> Aubl. (Anacardiaceae). (<i>B</i>) Tettigoniidae sp.4. (Orthoptera) on leaves of <i>Guatteria dumetorum</i> R. E. Fr (Annonaceae). (<i>C</i>) <i>Atta</i> sp.1 (Hymenoptera: Formicidae) on leaflets of <i>Jacaranda copaia</i> (Aubl.) D. Don (Bignoniaceae) causing margin feeding DT13. (<i>D</i>) Hole and margin feeding DT05, DT12 on leaves of <i>Manilkara bidentata</i> (A. DC.) A. Chev. (Sapotaceae) induced by Tettigoniidae sp.5 (Orthoptera). Sample 09-216. (<i>E</i>) Margin feeding DT12 and skeletonization DT22 on leaves of <i>Vochysia ferruginea</i> Mart. (Vochysiaceae) induced by multidamaging species Cryptocephalinae sp.1 (Coleoptera: Chrysomelidae). Sample 09-131. (<i>F</i>) Surface feeding damage DT30 on leaf of <i>T. guianensis</i>, inflicted by monodamaging species <i>Homeolabus analis</i> Illiger (Coleoptera: Attelabidae). Sample 09-135.</p

The Butterflies of Barro Colorado Island, Panama: Local Extinction since the 1930s

<div><p>Few data are available about the regional or local extinction of tropical butterfly species. When confirmed, local extinction was often due to the loss of host-plant species. We used published lists and recent monitoring programs to evaluate changes in butterfly composition on Barro Colorado Island (BCI, Panama) between an old (1923–1943) and a recent (1993–2013) period. Although 601 butterfly species have been recorded from BCI during the 1923–2013 period, we estimate that 390 species are currently breeding on the island, including 34 cryptic species, currently only known by their DNA Barcode Index Number. Twenty-three butterfly species that were considered abundant during the old period could not be collected during the recent period, despite a much higher sampling effort in recent times. We consider these species locally extinct from BCI and they conservatively represent 6% of the estimated local pool of resident species. Extinct species represent distant phylogenetic branches and several families. The butterfly traits most likely to influence the probability of extinction were host growth form, wing size and host specificity, independently of the phylogenetic relationships among butterfly species. On BCI, most likely candidates for extinction were small hesperiids feeding on herbs (35% of extinct species). However, contrary to our working hypothesis, extinction of these species on BCI cannot be attributed to loss of host plants. In most cases these host plants remain extant, but they probably subsist at lower or more fragmented densities. Coupled with low dispersal power, this reduced availability of host plants has probably caused the local extinction of some butterfly species. Many more bird than butterfly species have been lost from BCI recently, confirming that small preserves may be far more effective at conserving invertebrates than vertebrates and, therefore, should not necessarily be neglected from a conservation viewpoint.</p></div

The Butterflies of Barro Colorado Island, Panama: Local Extinction since the 1930s - Fig 1

<p>(a) Cumulative the number of individuals collected/observed plotted against the mean cumulative number of species collected/observed, for the recent period (1993–2013). Inset: cumulative no. of CTFS transects performed in the shady understory of BCI (2008–2013) plotted against the mean cumulative number of species collected/observed. Broken lines are 95% C.L. (b) Cumulative no. of individuals sequenced plotted against the cumulative no. of cryptic species discovered, for years 2008–2012. The grey line represents the best fit model, with its equation in inset.</p

Details of the % distribution of species richness within the 9 categories of abundance status

<p>(<a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0136623#pone.0136623.t002" target="_blank">Table 2</a>) ordered by (a) faunal composition by families; (b) indices of host specificity; (c) host growth form; (d) indices of geographic distribution; (e) wing color pattern; and (f) wing size. For definition of (b), (d) and (e) indices, see <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0136623#pone.0136623.s011" target="_blank">S1 Text</a>.</p

Datasets used to compile a list of butterfly species collected or observed on BCI, 1923–2013.

<p>(*) Lycaenidae only. All records coded with year 1974, being the mid-point of 1962–1986, this period corresponding to the stay of G. Small in Panama.</p><p>(**) All records coded with year 2000, being the “mid-point” of 1996–2005.</p><p>The number of records (individuals) are indicated for the old and recent periods, as well as for the entire period of study.</p

Plot of the scores of sampling years in axes 1 and 2 of the NMDS.

<p>Years are linked chronologically by a solid line. Pie charts indicate for each year the proportion of abundance accounted by (in clockwise order) Hesperiidae (black), Lycaenidae (white), Nymphalidae (grey), Papilionidae (black stippled), Pieridae (white stippled) and Riodinidae (grey squared).</p

A maximum clade credibility consensus tree depicting the phylogenetic relationships between 451 butterfly taxa from six families (see text for details).

<p>Taxa marked in red (actual BIN used) or orange (replacement congeneric BIN used) represent taxa that were abundant in the 1923–1943 surveys but that were not found in the 1993–2013 surveys. Scale bar in millions of years.</p