Acknowledging uncertainty in evolutionary reconstructions of ecological niches

Reconstructing ecological niche evolution can provide insight into the biogeography and diversification of evolving lineages. However, comparative phylogenetic methods may infer the history of ecological niche evolution inaccurately because (a) species' niches are often poorly characterized; and (b) phylogenetic comparative methods rely on niche summary statistics rather than full estimates of species' environmental tolerances. Here, we propose a new framework for coding ecological niches and reconstructing their evolution that explicitly acknowledges and incorporates the uncertainty introduced by incomplete niche characterization. Then, we modify existing ancestral state inference methods to leverage full estimates of environmental tolerances. We provide a worked empirical example of our method, investigating ecological niche evolution in the New World orioles (Aves: Passeriformes: Icterus spp.). Temperature and precipitation tolerances were generally broad and conserved among orioles, with niche reduction and specialization limited to a few terminal branches. Tools for performing these reconstructions are available in a new R package called nichevol.     

Competition and Facilitation in the Capuchin–Squirrel Monkey Relationship

In Guyana, the range of the brown capuchin, Cebus apella, meets the range of its congener, the wedge‐capped capuchin, C. olivaceus, with the two species exhibiting a mutually exclusive patchy distribution. Squirrel monkeys, Saimiri sciureus, and C. apella form ubiquitous interspecific associations, but the reason remains debatable. With a large biogeographic field study, we tested the degree to which the distribution and abundance of Cebus and S. sciureus is determined by habitat type, fruit availability, and geography (i.e., determinants of the fundamental niche) relative to interspecific interactions, such as competition and facilitation (i.e., the realized niche). We used the competition between the two capuchin monkeys as a natural experiment that subjected S. sciureus to C. apella and C. olivaceus ‘treatments’. Using spatial regression models and principal components analysis, we found that S. sciureus was associated with seasonally flooded forests, and was correlated with fruit abundance and diversity (fundamental niche), but was also correlated with C. apella density even when accounting for habitat and fruit availability (realized niche). Saimiri sciureus density was unrelated to C. olivaceus density. Cebus apella was associated with a variety of forest types, but particularly included disturbed and edge habitats such as logged forests, seasonally flooded forests, and upland savanna, in addition to mature forest. Cebus apella was also positively correlated with S. sciureus density and negatively correlated with the density of C. olivaceus. In contrast, C. olivaceus avoided riparian areas and was associated with mixed‐height forests on sloped mountainous terrain. In sum, interspecific interactions such as competition between species of Cebus and facilitation between C. apella and S. sciureus were as important as habitat and fruit availability in determining the distribution and abundance of these primates.     

Contrasting effects of high‐intensity photosynthetically active radiation on two bloom‐forming dinoflagellates

While light limitation can inhibit bloom formation in dinoflagellates, the potential for high‐intensity photosynthetically active radiation (PAR) to inhibit blooms by causing stress or damage has not been well‐studied. We measured the effects of high‐intensity PAR on the bloom‐forming dinoflagellates Alexandrium fundyense and Heterocapsa rotundata. Various physiological parameters (photosynthetic efficiency F_v/F_m, cell permeability, dimethylsulfoniopropionate [DMSP], cell volume, and chlorophyll‐a content) were measured before and after exposure to high‐intensity natural sunlight in short‐term light stress experiments. In addition, photosynthesis‐irradiance (P‐E) responses were compared for cells grown at different light levels to assess the capacity for photophysiological acclimation in each species. Experiments revealed distinct species‐specific responses to high PAR. While high light decreased F_v/F_m in both species, A. fundyense showed little additional evidence of light stress in short‐term experiments, although increased membrane permeability and intracellular DMSP indicated a response to handling. P‐E responses further indicated a high light‐adapted species with Chl‐a inversely proportional to growth irradiance and no evidence of photoinhibition; reduced maximum per‐cell photosynthesis rates suggest a trade‐off between photoprotection and C fixation in high light‐acclimated cells. Heterocapsa rotundata cells, in contrast, swelled in response to high light and sometimes lysed in short‐term experiments, releasing DMSP. P‐E responses confirmed a low light‐adapted species with high photosynthetic efficiencies associated with trade‐offs in the form of substantial photoinhibition and a lack of plasticity in Chl‐a content. These contrasting responses illustrate that high light constrains dinoflagellate community composition through species‐specific stress effects, with consequences for bloom formation and ecological interactions within the plankton.     

Improving our understanding of environmental controls on the distribution of C3 and C4 grasses

A number of studies have demonstrated the ecological sorting of C₃ and C₄ grasses along temperature and moisture gradients. However, previous studies of C₃ and C₄ grass biogeography have often inadvertently compared species in different and relatively unrelated lineages, which are associated with different environmental settings and distinct adaptive traits. Such confounded comparisons of C₃ and C₄ grasses may bias our understanding of ecological sorting imposed strictly by photosynthetic pathway. Here, we used MaxEnt species distribution modeling in combination with satellite data to understand the functional diversity of C₃ and C₄ grasses by comparing both large clades and closely related sister taxa. Similar to previous work, we found that C₄ grasses showed a preference for regions with higher temperatures and lower precipitation compared with grasses using the C₃ pathway. However, air temperature differences were smaller (2 °C vs. 4 °C) and precipitation and % tree cover differences were larger (1783 mm vs. 755 mm, 21.3% vs. 7.7%, respectively) when comparing C₃ and C₄ grasses within the same clade vs. comparing all C₄ and all C₃ grasses (i.e., ignoring phylogenetic structure). These results were due to important differences in the environmental preferences of C₃ BEP and PACMAD clades (the two main grass clades). Winter precipitation was found to be more important for understanding the distribution and environmental niche of C₃ PACMADs in comparison with both C₃ BEPs and C₄ taxa, for which temperature was much more important. Results comparing closely related C₃–C₄ sister taxa supported the patterns derived from our modeling of the larger clade groupings. Our findings, which are novel in comparing the distribution and niches of clades, demonstrate that the evolutionary history of taxa is important for understanding the functional diversity of C₃ and C₄ grasses, and should have implications for how grasslands will respond to global change.     

Capture efficiency and trophic adaptations of a specialist and generalist predator: A comparison

Specialist true predators are expected to exhibit higher capture efficiencies for the capture of larger and dangerous prey than generalist predators due to their possession of specialized morphological and behavioral adaptations. We used an araneophagous spider (Lampona murina) and a generalist spider (Drassodes lapidosus) as phylogenetically related model species and investigated their realized and fundamental trophic niches and their efficacy with respect to prey capture and prey handling. The trophic niche of both species confirmed that Lampona had a narrow trophic niche with a predominance of spider prey (including conspecifics), while the niche of Drassodes was wide, without any preference. DNA analysis of the gut contents of Lampona spiders collected in the field revealed that spiders form a significant part of its natural diet. Lampona captured significantly larger prey than itself and the prey captured by Drassodes. As concerns hunting strategy, Lampona grasped the prey with two pairs of legs possessing scopulae, whereas Drassodes immobilized prey with silk. Lampona possess forelegs equipped with scopulae and a thicker cuticle similar to other nonrelated araneophagous spiders. Lampona fed for a longer time and extracted more nutrients than Drassodes. We show that specialized behavioral and morphological adaptations altogether increase the hunting efficiency of specialists when compared to generalists.     

Influence of niche similarity on hybridization between Myriophyllum sibiricum and M. spicatum

The impact of ecological factors on natural hybridization is of widespread interest. Here, we asked whether climate niche influences hybridization between the two closely related plant species Myriophyllum sibiricum and M. spicatum. Eight microsatellite loci and two chloroplast fragments were used to investigate the occurrence of hybridization between these two species in two co‐occurring regions: north‐east China (NEC) and the Qinghai‐Tibetan Plateau (QTP). The climate niches of the species were quantified by principal component analysis with bioclimatic data, and niche comparisons were performed between the two species in each region. Reciprocal hybridization was observed, and M. sibiricum was favoured as the maternal species. Furthermore, hybrids were rare in NEC but common in the QTP. Accordingly, in NEC, the two species were climatically distinct, and hybrids only occurred in the narrow geographical or ecological transition zone, whereas in the QTP, obvious niche overlaps were found for the two species, and hybrids occurred in multiple contact zones. This association between hybridization pattern and climate niche similarity suggests that the level of hybridization was promoted by niche overlap. Compared with the parental species, similar climate niches were found for the hybrid populations in the QTP, indicating that other environmental factors rather than climate were important for hybrid persistence. Our findings highlight the significance of climate niche with respect to hybridization patterns in plants.     

Morphological convergence in a Mexican garter snake associated with the ingestion of a novel prey

Morphological convergence is expected when organisms which differ in phenotype experience similar functional demands, which lead to similar associations between resource utilization and performance. To consume prey with hard exoskeletons, snakes require either specialized head morphology, or to deal with them when they are vulnerable, for example, during molting. Such attributes may in turn reduce the efficiency with which they prey on soft‐bodied, slippery animals such as fish. Snakes which consume a range of prey may present intermediate morphology, such as that of Thamnophiine (Natricinae), which may be classified morphometrically across the soft–hard prey dietary boundary. In this study, we compared the dentition and head structure of populations of Thamnophis melanogaster that have entered the arthropod–crustacean (crayfish)‐eating niche and those that have not, and tested for convergence between the former and two distantly related crayfish specialists of the genus Regina (R. septemvittata and R. grahamii). As a control, we included the congener T. eques. Multivariate analysis of jaw length, head length, head width, and number of maxillary teeth yielded three significant canonical variables that together explained 98.8% of the variance in the size‐corrected morphological data. The first canonical variable significantly discriminated between the three species. The results show that head dimensions and number of teeth of the two Regina species are more similar to those of crayfish‐eating T. melanogaster than to non‐crayfish‐eating snakes or of T. eques. It is unclear how particular head proportions or teeth number facilitates capture of crayfish, but our results and the rarity of soft crayfish ingestion by T. melanogaster may reflect the novelty of this niche expansion, and are consistent with the hypothesis that some populations of T. melanogaster have converged in their head morphology with the two soft crayfish‐eating Regina species, although we cannot rule out the possibility of a morphological pre‐adaptation to ingest crayfish.     

Age‐related variation in the trophic characteristics of a marsupial carnivore,the Tasmanian devil Sarcophilus harrisii

Age‐related changes in diet have implications for competitive interactions and for predator–prey dynamics, affecting individuals and groups at different life stages. To quantify patterns of variation and ontogenetic change in the diets of Tasmanian devils Sarcophilus harrisii, a threatened marsupial carnivore, we analyzed variation in the stable isotope composition of whisker tissue samples taken from 91 individual devils from Wilmot, Tasmania from December 2014 to February 2017. Both δ¹³C and δ¹⁵N decreased with increasing age in weaned Tasmanian devils, indicating that as they age devils rely less on small mammals and birds, and more on large herbivores. Devils <12 months old had broader group isotopic niches, as estimated by Bayesian standard ellipses (SEA_B mode = 1.042) than devils from 12 to 23 months old (mode = 0.541) and devils ≥24 months old (mode = 0.532). Devils <24 months old had broader individual isotopic niches (SEA_B mode range 0.492–1.083) than devils ≥24 months old (mode range 0.092–0.240). A decrease in δ¹⁵N from the older whisker sections to the more recently grown sections in devils <24 months old likely reflects the period of weaning in this species, as this pattern was not observed in devils ≥24 months old. Our data reveal changes in the isotopic composition of devil whiskers with increasing age, accompanied by a reduction in isotopic variation both among population age classes and within individuals, reflecting the effect of weaning in early life, and a likely shift from an initially diverse diet of small mammals, birds, and invertebrates towards increasing consumption of larger herbivores in adulthood.     

Trophodynamics of Southern Ocean pteropods on the southern Kerguelen Plateau

Pteropods are a group of small marine gastropods that are highly sensitive to multiple stressors associated with climate change. Their trophic ecology is not well studied, with most research having focused primarily on the effects of ocean acidification on their fragile, aragonite shells. Stable isotopes analysis coupled with isotope‐based Bayesian niche metrics is useful for characterizing the trophic structure of biological assemblages. These approaches have not been implemented for pteropod assemblages. We used isotope‐based Bayesian niche metrics to investigate the trophic relationships of three co‐occurring pteropod species, with distinct feeding behaviors, sampled from the Southern Kerguelen Plateau area in the Indian Sector of the Southern Ocean—a biologically and economically important but poorly studied region. Two of these species were gymnosomes (shell‐less pteropods), which are traditionally regarded as specialist predators on other pteropods, and the third species was a thecosome (shelled pteropod), which are typically generalist omnivores. For each species, we aimed to understand (a) variability and overlap among isotopic niches; and (b) whether there was a relationship between body size and trophic position. Observed isotopic niche areas were broadest for gymnosomes, especially Clione limacina antarctica, whose observed isotopic niche area was wider than expected on both δ¹³C and δ¹⁵N value axes. We also found that trophic position significantly increased with increasing body length for Spongiobranchaea australis. We found no indication of a dietary shift toward increased trophic position with increasing body size for Clio pyramidata f. sulcata. Trophic positions ranged from 2.8 to 3.5, revealing an assemblage composed of both primary and secondary consumer behaviors. This study provides a comprehensive comparative analysis on trophodynamics in Southern Ocean pteropod species, and supports previous studies using gut content, fatty acid and stable isotope analyses. Combined, our results illustrate differences in intraspecific trophic behavior that may be attributed to differential feeding strategies at species level.     

Using maximum entropy to predict the potential distribution of an invasive freshwater snail

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Divergent habitat use of two urban lizard species

Faunal responses to anthropogenic habitat modification represent an important aspect of global change. In Puerto Rico, two species of arboreal lizard, Anolis cristatellus and A. stratulus, are commonly encountered in urban areas, yet seem to use the urban habitat in different ways. In this study, we quantified differences in habitat use between these two species in an urban setting. For each species, we measured habitat use and preference, and the niche space of each taxon, with respect to manmade features of the urban environment. To measure niche space of these species in an urban environment, we collected data from a total of six urban sites across four different municipalities on the island of Puerto Rico. We quantified relative abundance of both species, their habitat use, and the available habitat in the environment to measure both microhabitat preference in an urban setting, as well as niche partitioning between the two different lizards. Overall, we found that the two species utilize different portions of the urban habitat. Anolis stratulus tends to use more “natural” portions of the urban environment (i.e., trees and other cultivated vegetation), whereas A. cristatellus more frequently uses anthropogenic structures. We also found that aspects of habitat discrimination in urban areas mirror a pattern measured in prior studies for forested sites in which A. stratulus was found to perch higher than A. cristatellus and preferred lower temperatures and greater canopy cover. In our study, we found that the multivariate niche space occupied by A. stratulus did not differ from the available niche space in natural portions of the urban environment and in turn represented a subset of the niche space occupied by A. cristatellus. The unique niche space occupied by A. cristatellus corresponds to manmade aspects of the urban environment generally not utilized by A. stratulus. Our results demonstrate that some species are merely tolerant of urbanization while others utilize urban habitats in novel ways. This finding has implications for long‐term persistence in urban habitats and suggests that loss of natural habitat elements may lead to nonrandom species extirpations as urbanization intensifies.