Rui Rebelo

Colonization of freshwater habitats by an introduced crayfish, Procambarus clarkii, in Southwest Iberian Peninsula

The introduction of some crustacean species has produced alterations of freshwater environments and declines of native species worldwide. The red swamp crayfish, Procambarus clarkii Girard, was introduced in the Southwest Iberian Peninsula in the 1970’s, producing severe impacts on rice agriculture and on native biota such as macrophytes, gastropods, native crayfish and amphibians. We studied the distribution of P. clarkii in two areas of SW Iberian Peninsula: the Sado River basin (SW Portugal), an area colonized by this species around 1990, and the Parque Natural del Entorno de Doñana (SW Spain), colonized soon after its introduction in the Iberian Peninsula, in the 1970’s. Our main goal was to determine which factors limit crayfish distribution, which could help to identify the most effective management practices to contain its spread. Procambarus clarkii was found in most types of water bodies, including small and shallow ones. Distance to a crayfish source was the single predictor variable explaining crayfish occurrence in most types of habitats and in both areas. The only exception was for the Sado permanent stream points, where crayfish presence was negatively affected by an interaction between elevation and flow velocity. Other habitat characteristics have apparently little or no importance for its successful colonization. Moreover, this study indicated that overland dispersal is apparently a frequent phenomenon in this species. Our findings can be used to determine which habitats are most likely to be colonized by the crayfish and to develop practical measures which may limit its spread and minimize its impacts.

Vulnerability of Southwest Iberian amphibians to an introduced crayfish, Procambarus clarkii

The introduction of predators in amphibian breeding habitats may contribute to the decline or extinction of amphibian populations. Procambarus clarkii , a North American crayfish, was recently introduced in the Iberian Peninsula, being now quite abundant in the southwest, a region with no native crayfish species and where 13 amphibian species may be found. We performed mesocosm experiments to evaluate the vulnerability of amphibian embryos and larvae from those species to P. clarkii . Despite the presence of alternative food (vegetation and leaf litter), embryo survival in the presence of P. clarkii was low for all species except Bufo bufo . However, newly hatched B. bufo tadpoles were readily consumed. P. clarkii reduced larval survival in all species, with those species that in nature have few contacts with predators at the larval stage suffering the highest mortalities. Most larvae reduced their activity and/or altered microhabitat use in the presence of P. clarkii , but these behavioural modifications did not lead necessarily to a low vulnerability to predation.

Numbers and population trends of Cory’s Shearwater Calonectris diomedea at Selvagem Grande, Northeast Atlantic

Abstract The island of Selvagem Grande holds one of the most important colonies of Cory’s Shearwater (Calonectris diomedea) in the Atlantic. Historical records suggest a stable population well in excess of 100,000 pairs. A succession of massacres in 1975 and 1976 dramatically reduced this population to less than 10% of the original numbers. Since 1977 strict protection was enforced and the population started a steady recovery. However, between 1995 and 1998 an alarming decline, of more than 13% of the birds, was reported and concurrently the monitoring work was interrupted. Data from other colonies in the Atlantic and the Mediterranean also indicated significant regional declines, some of which appear to be driven by unsustainable levels of accidental mortality in fishing gear. In order to investigate the persistence of the regressive trend at Selvagem Grande, we carried out a global census of the colony in June 2005. We counted 20,555 occupied nests and estimated the total breeding population at 29,540 pairs. The population still appears to be recovering from the massacres of 1975-1976, at an average rate of about 4.6% per year over the past 25 years. Our data reveal that Selvagem Grande now harbors the largest known Cory’s Shearwater colony in the World. Results from this study suggest that this population is not, as yet, suffering from unsustainable fisheries-related mortality, which would be reflected in a decline in numbers. This situation contrasts with that of the Mediterranean, where significant mortality in fishing gear has been linked to shearwater population declines.

Do anuran larvae respond behaviourally to chemical cues from an invasive crayfish predator? A community-wide study.

Antipredator behaviour is an important fitness component in most animals. A co-evolutionary history between predator and prey is important for prey to respond adaptively to predation threats. When non-native predator species invade new areas, native prey may not recognise them or may lack effective antipredator defences. However, responses to novel predators can be facilitated by chemical cues from the predators’ diet. The red swamp crayfish Procambarus clarkii is a widespread invasive predator in the Southwest of the Iberian Peninsula, where it preys upon native anuran tadpoles. In a laboratory experiment we studied behavioural antipredator defences (alterations in activity level and spatial avoidance of predator) of nine anurans in response to P. clarkii chemical cues, and compared them with the defences towards a native predator, the larval dragonfly Aeshna sp. To investigate how chemical cues from consumed conspecifics shape the responses, we raised tadpoles with either a tadpole-fed or starved crayfish, or dragonfly larva, or in the absence of a predator. Five species significantly altered their behaviour in the presence of crayfish, and this was largely mediated by chemical cues from consumed conspecifics. In the presence of dragonflies, most species exhibited behavioural defences and often these did not require the presence of cues from predation events. Responding to cues from consumed conspecifics seems to be a critical factor in facilitating certain behavioural responses to novel exotic predators. This finding can be useful for predicting antipredator responses to invasive predators and help directing conservation efforts to the species at highest risk.

Predation by an Exotic Crayfish, Procambarus clarkii, on Natterjack Toad, Bufo calamita, Embryos: Its Role on the Exclusion of this Amphibian from its Breeding Ponds

Abstract Procambarus clarkii, an American crayfish, was introduced in the SW Iberian Peninsula three decades ago. This region has no native crayfishes; therefore, P. clarkii constitutes a potential threat for the embryos and larvae of amphibians, which may lack evolved defenses against it. We assessed the effects of this crayfish on the Natterjack Toad, Bufo calamita, using two complementary approaches. First, we studied the effect of crayfish presence on B. calamita breeding habitat use in temporary ponds of Doñana Natural Park (southwestern Spain). We surveyed 31 temporary ponds for the presence of P. clarkii and B. calamita eggs and tadpoles, and we conducted a logistic regression to determine if crayfish were significantly associated with Natterjack Toad distribution after habitat variables were taken into account. Second, we experimentally evaluated the impact of P. clarkii on B. calamita embryos in natural ponds with a two × two factorial experiment, using two ponds (one with and one without crayfish) and two treatments (embryos exposed or not exposed to predators). Crayfish presence was a negative predictor of B. calamita breeding habitat use; co-occurrence of the two species was limited to only one pond. Moreover, the predation experiment showed that survival of B. calamita embryos was strikingly reduced when they were directly exposed to crayfish compared to survival in all other treatments. Our results indicated that P. clarkii has a strong effect on B. calamita reproductive success and that it may play an important role in structuring amphibian communities in temporary ponds.

Rapid evolution of constitutive and inducible defenses against an invasive predator

Invasive alien predators can impose strong selection on native prey populations and induce rapid evolutionary change in the invaded communities. However, studies on evolutionary responses to invasive predators are often complicated by the lack of replicate populations differing in coexistence time with the predator, which would allow the determination of how prey traits change during the invasion. The red swamp crayfish Procambarus clarkii has invaded many freshwater areas worldwide, with negative impacts for native fauna. Here, we examined how coexistence time shapes antipredator responses of the Iberian waterfrog (Pelophylax perezi) to the invasive crayfish by raising tadpoles from five populations differing in historical exposure to P. clarkii (30 years, 20 years, or no coexistence). Tadpoles from non-invaded populations responded to the presence of P. clarkii with behavioral plasticity (reduced activity), whereas long-term invaded populations showed canalized antipredator behavior (constant low activity level). Tadpoles from one of the long-term invaded populations responded to the crayfish with inducible morphological defenses (deeper tails), reflecting the use of both constitutive and inducible antipredator defenses against the exotic predator by this population. Our results suggest that, while naive P. perezi populations responded behaviorally to P. clarkii, the strong predation pressure imposed by the crayfish has induced the evolution of qualitatively different antipredator defenses in populations with longer coexistence time. These responses suggest that strong selection by invasive predators may drive rapid evolutionary change in invaded communities. Examining responses of prey species to biological invasions using multiple populations will help us better forecast the impact of invasive predators in natural communities.

Site Tenacity in the Terrestrial Salamandrid Salamandra salamandra

Abstract A six-year capture-recapture study allowed us to assess site-tenacity and spatial distribution of site-tenacious individuals in a population of the terrestrial, ovoviviparous Salamandra salamandra from Sintra-Cascais Natural Park, Portugal. The study area, an abandoned orchard, maintained large numbers of S. salamandra (about 400/ha). Most site-tenacious individuals were associated with tunnels in old stone walls that supported former agricultural terraces. Age was the only trait that explained site-tenacity in both sexes. The number of residents in each wall was positively related with wall length, and the sex-ratio of the residents was approximately 1:1 in every wall. Several animals spent all of the study period in the same area.

How consumption and fragmentation of macrophytes by the invasive crayfish Procambarus clarkii shape the macrophyte communities of temporary ponds.

Crayfish are major herbivores in freshwaters, and their activity may change invaded freshwater ecosystems. Macrophyte removal by crayfish results from consumption and fragmentation of plant material and may depend upon the palatability of each species. We studied the impact of Procambarus clarkii on the macrophyte community of Mediterranean temporary ponds, testing in laboratory if consumption and fragmentation of five macrophyte species were correlated in palatability tests and in a preference test. We performed an experiment in a natural pond, where we introduced crayfish and estimated its effects on macrophyte biomass, number of rooted stalks and number of floating cut stalks. P. clarkii consumed preferably Juncus heterophyllus in both tests and avoided Carex divisa and Ranunculus peltatus in the preference test. In the presence of preferred species, consumption and fragmentation of the non-preferred species were heavily reduced. In the field trial, the “Crayfish” compartment had 31% less macrophyte biomass, 41% less rooted stalks and 92% more floating cut stalks. Crayfish may remove macrophyte species from the community sequentially, from the most to the least preferred species. Impacts of crayfish in temporary ponds may depend on time of invasion and on the composition of the macrophyte community.

Evaluating green infrastructure in urban environments using a multi-taxa and functional diversity approach.

Forested areas within cities host a large number of species, responsible for many ecosystem services in urban areas. The biodiversity in these areas is influenced by human disturbances such as atmospheric pollution and urban heat island effect. To ameliorate the effects of these factors, an increase in urban green areas is often considered sufficient. However, this approach assumes that all types of green cover have the same importance for species. Our aim was to show that not all forested green areas are equal in importance for species, but that based on a multi-taxa and functional diversity approach it is possible to value green infrastructure in urban environments. After evaluating the diversity of lichens, butterflies and other-arthropods, birds and mammals in 31 Mediterranean urban forests in south-west Europe (Almada, Portugal), bird and lichen functional groups responsive to urbanization were found. A community shift (tolerant species replacing sensitive ones) along the urbanization gradient was found, and this must be considered when using these groups as indicators of the effect of urbanization. Bird and lichen functional groups were then analyzed together with the characteristics of the forests and their surroundings. Our results showed that, contrary to previous assumptions, vegetation density and more importantly the amount of urban areas around the forest (matrix), are more important for biodiversity than forest quantity alone. This indicated that not all types of forested green areas have the same importance for biodiversity. An index of forest functional diversity was then calculated for all sampled forests of the area. This could help decision-makers to improve the management of urban green infrastructures with the goal of increasing functionality and ultimately ecosystem services in urban areas.

Morphological and life‐history responses of anurans to predation by an invasive crayfish: an integrative approach

Predator-induced phenotypic plasticity has been widely documented in response to native predators, but studies examining the extent to which prey can respond to exotic invasive predators are scarce. As native prey often do not share a long evolutionary history with invasive predators, they may lack defenses against them. This can lead to population declines and even extinctions, making exotic predators a serious threat to biodiversity. Here, in a community-wide study, we examined the morphological and life-history responses of anuran larvae reared with the invasive red swamp crayfish, Procambarus clarkii, feeding on conspecific tadpoles. We reared tadpoles of nine species until metamorphosis and examined responses in terms of larval morphology, growth, and development, as well as their degree of phenotypic integration. These responses were compared with the ones developed in the presence of a native predator, the larval dragonfly Aeshna sp., also feeding on tadpoles. Eight of the nine species altered their morphology or life history when reared with the fed dragonfly, but only four when reared with the fed crayfish, suggesting among-species variation in the ability to respond to a novel predator. While morphological defenses were generally similar across species (deeper tails) and almost exclusively elicited in the presence of the fed dragonfly, life-history responses were very variable and commonly elicited in the presence of the invasive crayfish. Phenotypes induced in the presence of dragonfly were more integrated than in crayfish presence. The lack of response to the presence of the fed crayfish in five of the study species suggests higher risk of local extinction and ultimately reduced diversity of the invaded amphibian communities. Understanding how native prey species vary in their responses to invasive predators is important in predicting the impacts caused by newly established predator–prey interactions following biological invasions.