Deep impact: in situ functional responses reveal context-dependent interactions between vertically migrating invasive and native mesopredators and shared prey

The ecological effects of invasive species depend on myriad environmental contexts, rendering understanding problematic. Functional responses provide a means to quantify resource use by consumers over short timescales and could therefore provide insight into how the effects of invasive species vary over space and time. Here, we use novel in situ microcosm experiments to track changes in the functional responses of two aquatic mesopredators, one native and the other an invader, as they undergo diel vertical migrations through a lake water column.
The Ponto–Caspian mysid, Hemimysis anomala, a known ecologically damaging invader, generally had higher a functional response towards cladoceran prey than did a native trophic analogue, Mysis salemaai. However, this differential was spatiotemporally dependent, being minimal during the day on the lake bottom, and increasing at night, particularly inshore.
Because the functional response of the native predator was spatiotemporally consistent, the above pattern was driven by changes in the invader functional response over the diel cycle. In particular, the functional response of H. anomala was significantly reduced on the lake bottom during the daytime relative to night, and predation was especially pronounced in shallow surface waters.
We demonstrate the context dependency of the effects of an invasive predator on prey populations and emphasise the utility of functional responses as tools to inform our understanding of predator–prey interactions. In situ manipulations integrate experimental rigour with field relevance and have the potential to reveal how impacts manifest over a range of spatiotemporal scales.

Predicting the predatory impacts of the “demon shrimp” Dikerogammarus haemobaphes, on native and previously introduced species

Biological invasions continue to exert pressure on ecosystems worldwide and we thus require methods that can help understand and predict the impacts of invasive species, on both native species and previously established invaders. Comparing laboratory derived functional responses among invasive and native predators has emerged as one such method, providing a robust proxy for field impacts. We used this method to examine the likely impacts of the Ponto–Caspian amphipod Dikerogammarus haemobaphes, known as the “demon shrimp”, a little investigated invader in European freshwaters that has recently established in the British Isles. We compared the functional responses on two prey species of D. haemobaphes with two other amphipod species: Dikerogammarus villosus, a congeneric invasive with well-documented impacts on macro-invertebrate communities and a native amphipod, Gammarus pulex. Prey species were native Chironomus sp. and the invasive Chelicorophium curvispinum, a tube-building amphipod also originating from the Ponto–Caspian region. D. villosus showed higher Type II functional responses towards both prey species than did D. haemobaphes and G. pulex, with the latter two predators exhibiting similar impacts on the native prey. However, D. haemobaphes had higher functional responses towards the invasive C. curvispinum than did G. pulex, both when prey individuals were tubeless and resident in their protective mud tubes. Thus, we demonstrate that functionally equivalent invasive congeners can show significantly different impacts on prey, regardless of shared evolutionary history. We also show that some predatory invaders can have impacts on native prey equivalent to native predator impacts, but that they can also exert significant impacts on previously introduced prey. We discuss the importance of invasion history and prey identity when attempting to understand and predict the impacts of new invaders.

Coexistence of congeneric native and invasive species: The case of the green algae Codium spp. in northwestern Spain

We examined the patterns of distribution and abundance, and reproductive traits (presence of gametophytes and size at time of reproduction) in the invasive Codium fragile ssp. fragile and the native C. tomentosum and C. vermilara on intertidal habitats of NW Spain at two dates. All three species coexist in the locations and habitats studied, although abundances were low. We found a greater proportion of C. fragile ssp. fragile towards the east of the Cantabrian coast and on upper levels on the shore, where conditions are more stressful. The proportion of thalli bearing gametangia in C. fragile ssp. fragile was greater than in the native species in all habitats. The presence of gametangia was size-dependent for all species, with the invasive species maturing at a smaller size, which combined with the previous features, might confer competitive advantages to this species over the native species. We also demonstrated that molecular analyses are necessary for the correct identification of C. fragile subspecies.

Range expansion and comparative habitat use of insular, congeneric lagomorphs: invasive European hares Lepus europaeus and endemic Irish hares Lepus timidus hibernicus

The European hare (Lepus europaeus) has declined throughout its native range but invaded numerous regions where it has negatively impacted native wildlife. In southern Sweden, it replaces the native mountain hare (L. timidus) through competition and hybridisation. We investigated temporal change in the invasive range of the European hare in Ireland, and compared its habitat use with the endemic Irish hare (L. timidus hibernicus). The range of the European hare was three times larger and its core range twice as large in 2012–2013 than in 2005. Its rate of radial range expansion was 0.73 km year−1 with its introduction estimated to have occurred ca. 1970. Both species utilised improved and rough grasslands and exhibited markedly similar regression coefficients with almost every land cover variable examined. Irish hares were associated with low fibre and high sugar content grass (good quality grazing) whilst the invader had a greater tolerance for low quality forage. European hares were associated with habitat patch edge density, suggesting it may be more suited to using hedgerows as diurnal resting sites than the Irish hare. Consequently, the invader had a wider niche breadth than the native but their niche overlap was virtually complete. Given the impact of the European hare on native species elsewhere, and its apparent pre-adaption for improved grasslands interspersed with arable land (a habitat that covers 70 % of Ireland), its establishment and range expansion poses a significant threat to the ecological security of the endemic Irish hare, particularly given their ecological similarities.

Conduit artery structure and function in lowlanders and native highlanders: relationships with oxidative stress and role of sympathoexcitation

Research detailing the normal vascular adaptions to high altitude is minimal and often confounded by pathology (e.g. chronic mountain sickness) and methodological issues. We examined vascular function and structure in: (1) healthy lowlanders during acute hypoxia and prolonged (∼2 weeks) exposure to high altitude, and (2) high-altitude natives at 5050 m (highlanders). In 12 healthy lowlanders (aged 32 ± 7 years) and 12 highlanders (Sherpa; 33 ± 14 years) we assessed brachial endothelium-dependent flow-mediated dilatation (FMD), endothelium-independent dilatation (via glyceryl trinitrate; GTN), common carotid intima–media thickness (CIMT) and diameter (ultrasound), and arterial stiffness via pulse wave velocity (PWV; applanation tonometry). Cephalic venous biomarkers of free radical-mediated lipid peroxidation (lipid hydroperoxides, LOOH), nitrite (NO₂^–) and lipid soluble antioxidants were also obtained at rest. In lowlanders, measurements were performed at sea level (334 m) and between days 3–4 (acute high altitude) and 12–14 (chronic high altitude) following arrival to 5050 m. Highlanders were assessed once at 5050 m. Compared with sea level, acute high altitude reduced lowlanders’ FMD (7.9 ± 0.4 vs. 6.8 ± 0.4%; P = 0.004) and GTN-induced dilatation (16.6 ± 0.9 vs. 14.5 ± 0.8%; P = 0.006), and raised central PWV (6.0 ± 0.2vs. 6.6 ± 0.3 m s⁻¹; P = 0.001). These changes persisted at days 12–14, and after allometrically scaling FMD to adjust for altered baseline diameter. Compared to lowlanders at sea level and high altitude, highlanders had a lower carotid wall:lumen ratio (∼19%, P ≤ 0.04), attributable to a narrower CIMT and wider lumen. Although both LOOH and NO₂^– increased with high altitude in lowlanders, only LOOH correlated with the reduction in GTN-induced dilatation evident during acute (n = 11, r = −0.53) and chronic (n = 7, r = −0.69; P ≤ 0.01) exposure to 5050 m. In a follow-up, placebo-controlled experiment (n = 11 healthy lowlanders) conducted in a normobaric hypoxic chamber (inspired O₂ fraction () = 0.11; 6 h), a sustained reduction in FMD was evident within 1 h of hypoxic exposure when compared to normoxic baseline (5.7 ± 1.6 vs. 8.0 ±1.3%; P < 0.01); this decline in FMD was largely reversed following α₁-adrenoreceptor blockade. In conclusion, high-altitude exposure in lowlanders caused persistent impairment in vascular function, which was mediated partially via oxidative stress and sympathoexcitation. Although a lifetime of high-altitude exposure neither intensifies nor attenuates the impairments seen with short-term exposure, chronic high-altitude exposure appears to be associated with arterial remodelling.

High temperature thermal stability studies of ultrathin Al2O3 layers deposited on native oxide and sulphur passivated InGaAs surfaces

High resolution synchrotron radiation core level photoemission measurements have been used to undertake a comparative study of the high temperature stability of ultrathin Al2O3 layers deposited by atomic layer deposition (ALD) on both sulphur passivated and native oxide covered InGaAs. The residual interfacial oxides between sulphur passivated InGaAs and the ultrathin Al2O3 layer can be substantially removed at high temperature (up to 700 °C) without impacting on the InGaAs stoichiometry while significant loss of indium was recorded at this temperature on the native oxide InGaAs surface.

Genetic provenance and best practice woodland management: a case study in native alder (Alnus glutinosa)

In recent years, the native woodlands of Europe, including those of Britain and Ireland, have increasingly come under threat from a range of biotic and abiotic factors, and are therefore a conservation priority demanding careful management in order to realise their inherent ecological and cultural benefits. Because the distribution of genetic variation across populations and regions is increasingly considered an important component of woodland management, we carried out a population genetic analysis on black alder (Alnus glutinosa) across Northern Ireland in order to inform “best practice” strategies. Our findings suggest that populations harbour high levels of genetic diversity, with very little differentiation between populations. Significant F IS values were observed in over half of the populations analysed, however, which could reflect inbreeding as a result of the patchy occurrence of alder in Northern Ireland, with scattered, favourable damp habitats being largely isolated from each other by extensive tracts of farmland. Although there is no genetic evidence to support the broad-scale implementation of tree seed zones along the lines of those proposed for native woodlands in Great Britain, we suggest that the localised occurrence of rare chloroplast haplotypes should be taken into account on a case-by-case basis. This, coupled with the identification of populations containing high genetic diversity and that are broadly representative of the region as a whole, will provide a sound genetic basis for woodland management, both in alder and more generally for species that exhibit low levels of genetic differentiation.

Differential ecological impacts of an invader and a native under environmental change are revealed by comparative functional responses.

Predicting the ecological impacts of damaging invasive species under relevant environmental contexts is a major challenge, for which comparative functional responses (the relationship between resource availability and consumer uptake rate) have great potential. Here, the functional responses of Gammarus pulex, an ecologically damaging invader in freshwaters in Ireland and other islands, were compared with those of a native trophic equivalent Gammarus duebeni celticus. Experiments were conducted at two dissolved oxygen concentrations (80 and 50 % saturation), representative of anthropogenic water quality changes, using two larval prey, blackfly (Simuliidae spp.) and mayfly (Baetis rhodani). Overall, G. pulex had higher Type II functional responses and hence predatory impacts than G. d. celticus and the functional responses of both predators were reduced by lowered oxygen concentration. However, this reduction was of lower magnitude for the invader as compared to the native. Further, the invader functional response at low oxygen was comparable to that of the native at high oxygen. Attack rates of the two predators were similar, with low oxygen reducing these attack rates, but this effect occurred more strongly for blackfly than mayfly prey. Handling times were significantly lower for the invader compared with the native, and significantly higher at low oxygen, however, the effect of lowered oxygen on handling times was minimal for the invader and pronounced for the native. Maximum feeding rates were significantly greater for the invader compared with the native, and significantly reduced at low oxygen, with this effect again lesser for the invader as compared to the native. The greater functional responses of the invader corroborate with its impacts on recipient macroinvertebrate communities when it replaces the native. Further, our experiments predict that the impact of the invader will be less affected than the native under altered oxygen regimes driven by anthropogenic influences.

Lower resting energy expenditure and fat oxidation in Native American and Hispanic infants born to mothers with diabetes

OBJECTIVE: To determine whether exposure to diabetes in utero affects resting energy expenditure (REE) and fuel oxidation in infants.

STUDY DESIGN: At 35 ± 5 days after birth, body composition and REE were measured in full-term offspring of Native American and Hispanic women with either well-controlled diabetes (13 girls, 11 boys) or normal healthy pregnancies (18 girls, 17 boys).

RESULTS: Control of dysglycemia during gestation in the women with diabetes mellitus met current clinical standards, shown by average glycated hemoglobin (5.9 ± 0.2%; 40.6 ± 2.3 mmol/mol). Infant body mass (offspring of women with diabetes: 4.78 ± 0.13, control offspring: 4.56 ± 0.08 kg) and body fatness (offspring of women with diabetes: 25.2 ± 0.6, control offspring: 24.2 ± 0.5 %) did not differ between groups. REE, adjusted for lean body mass, was 14% lower in offspring of women with diabetes (41.7 ± 2.3 kJ/h) than control offspring (48.6 ± 2.0, P = .025). Fat oxidation was 26% lower in offspring of women with diabetes (0.54 ± 0.05 g/h) than control offspring (0.76 ± 0.04, P < .01) but carbohydrate oxidation did not differ. Thus, fat oxidation accounted for a lower fraction of REE in the offspring of women with diabetes (49 ± 4%) than control offspring (60 ± 3%, P = .022). Mothers with diabetes were older and had higher prepregnancy body mass index than control mothers.

CONCLUSIONS: Well-controlled maternal diabetes did not significantly affect body mass or composition of offspring at 1-month old. However, infants with mothers with diabetes had reduced REE and fat oxidation, which could contribute to adiposity and future disease risk. Further studies are needed to assess the impact differences in age and higher prepregnancy body mass index.

Cord blood adipokines, neonatal anthropometrics and postnatal growth in offspring of Hispanic and Native American women with diabetes mellitus

BACKGROUND: Offspring of women with diabetes mellitus (DM) during pregnancy have a risk of developing metabolic disease in adulthood greater than that conferred by genetics alone. The mechanisms responsible are unknown, but likely involve fetal exposure to the in utero milieu, including glucose and circulating adipokines. The purpose of this study was to assess the impact of maternal DM on fetal adipokines and anthropometry in infants of Hispanic and Native American women.

METHODS: We conducted a prospective study of offspring of mothers with normoglycemia (Con-O; n = 79) or type 2 or gestational DM (DM-O; n = 45) pregnancies. Infant anthropometrics were measured at birth and 1-month of age. Cord leptin, high-molecular-weight adiponectin (HMWA), pigment epithelium-derived factor (PEDF) and C-peptide were measured by ELISA. Differences between groups were assessed using the Generalized Linear Model framework. Correlations were calculated as standardized regression coefficients and adjusted for significant covariates.

RESULTS: DM-O were heavier at birth than Con-O (3.7 ± 0.6 vs. 3.4 ± 0.4 kg, p = 0.024), but sum of skinfolds (SSF) were not different. At 1-month, there was no difference in weight, SSF or % body fat or postnatal growth between groups. Leptin was higher in DM-O (20.1 ± 14.9 vs. 9.5 ± 9.9 ng/ml in Con-O, p < 0.0001). Leptin was positively associated with birth weight (p = 0.0007) and SSF (p = 0.002) in Con-O and with maternal hemoglobin A1c in both groups (Con-O, p = 0.023; DM-O, p = 0.006). PEDF was positively associated with birth weight in all infants (p = 0.004). Leptin was positively associated with PEDF in both groups, with a stronger correlation in DM-O (p = 0.009). At 1-month, HMWA was positively associated with body weight (p = 0.004), SSF (p = 0.025) and % body fat (p = 0.004) across the cohort.

CONCLUSIONS: Maternal DM results in fetal hyperleptinemia independent of adiposity. HMWA appears to influence postnatal growth. Thus, in utero exposure to DM imparts hormonal differences on infants even without aberrant growth.

Using particle dispersal models to assist in the conservation and recovery of the overexploited native oyster (Ostrea edulis) in an enclosed sea lough

Oyster populations around the world have seen catastrophic decline which has been largely attributed to overexploitation, disease and pollution. While considerable effort and resources have been implemented into restoring these important environmental engineers, the success of oyster populations is often limited by poor understanding of site-specific dispersal patterns of propagules. Water-borne transport is a key factor controlling or regulating the dispersal of the larval stage of benthic marine invertebrates which have limited mobility. The distribution of the native oyster Ostrea edulis in Strangford Lough, Northern Ireland, together with their densities and population structure at subtidal and intertidal sites has been documented at irregular intervals between 1997 and 2013. This paper revisits this historical data and considers whether different prevailing environmental conditions can be used to explain the distribution, densities and population structure of O. edulis in Strangford Lough. The approach adopted involved comparing predictive 2D hydrodynamic models coupled with particle tracking to simulate the dispersal of oyster larvae with historical and recent field records of the distribution of both subtidal and intertidal, populations since 1995. Results from the models support the hypothesis that commercial stocks of O. edulis introduced into Strangford Lough in the 1990s resulted in the re-establishment of wild populations of oysters in the Northern Basin which in turn provided a potential source of propagules for subtidal populations. These results highlight that strategic site selection (while inadvertent in the case of the introduced population in 1995) for the re-introduction of important shellfish species can significantly accelerate their recovery and restoration.

An invasive-native mammalian species replacement process captured by camera trap survey random encounter models

Camera traps are used to estimate densities or abundances using capture-recapture and, more recently, random encounter models (REMs). We deploy REMs to describe an invasive-native species replacement process, and to demonstrate their wider application beyond abundance estimation. The Irish hare Lepus timidus hibernicus is a high priority endemic of conservation concern. It is threatened by an expanding population of non-native, European hares L. europaeus, an invasive species of global importance. Camera traps were deployed in thirteen 1 km squares, wherein the ratio of invader to native densities were corroborated by night-driven line transect distance sampling throughout the study area of 1652 km2. Spatial patterns of invasive and native densities between the invader’s core and peripheral ranges, and native allopatry, were comparable between methods. Native densities in the peripheral range were comparable to those in native allopatry using REM, or marginally depressed using Distance Sampling. Numbers of the invader were substantially higher than the native in the core range, irrespective of method, with a 5:1 invader-to-native ratio indicating species replacement. We also describe a post hoc optimization protocol for REM which will inform subsequent (re-)surveys, allowing survey effort (camera hours) to be reduced by up to 57% without compromising the width of confidence intervals associated with density estimates. This approach will form the basis of a more cost-effective means of surveillance and monitoring for both the endemic and invasive species. The European hare undoubtedly represents a significant threat to the endemic Irish hare.

Trait-Mediated Effects of Parasites on Invader-Native Interactions.

Parasites have a variety of behavioural effects on their hosts, which can in turn affect species with which the host interacts. Here we review how these trait-mediated indirect effects of parasites can alter the outcomes of invader-native interactions, illustrating with examples from the literature and with particular regard to the invader-native crustacean systems studied in our laboratories. Parasites may potentially inhibit or exacerbate invasions via their effects on host behaviour, in addition to their direct virulence effects on hosts. In several crustacean systems, we have found that parasites influence both host predation rates on intra- and inter-guild prey and host vulnerability to being preyed upon. These trait effects can theoretically alter invasion impact and patterns of coexistence, as they indirectly affect interactions between predators and prey with the potential for further ramifications to other species in the food web. The fitness consequences of parasite-induced trait-mediated effects are rarely considered in traditional parasitological contexts, but demand attention in the context of ecological communities. We can regard these trait effects as a form of cryptic virulence that only becomes apparent when hosts are examined in the context of the other species with which they interact.

Genetic structure, relationships and admixture with wild relatives in native pig breeds from Iberia and its islands

Background: Native pig breeds in the Iberian Peninsula are broadly classified as belonging to either the Celtic or the Mediterranean breed groups, but there are other local populations that do not fit into any of these groups. Most of the native pig breeds in Iberia are in danger of extinction, and the assessment of their genetic diversity and population structure, relationships and possible admixture between breeds, and the appraisal of conservation alternatives are crucial to adopt appropriate management strategies. Methods: A panel of 24 microsatellite markers was used to genotype 844 animals representing the 17 most important native swine breeds and wild populations existing in Portugal and Spain and various statistical tools were applied to analyze the results. Results: Genetic diversity was high in the breeds studied, with an overall mean of 13.6 alleles per locus and an average expected heterozygosity of 0.80. Signs of genetic bottlenecks were observed in breeds with a small census size, and population substructure was present in some of the breeds with larger census sizes. Variability among breeds accounted for about 20% of the total genetic diversity, and was explained mostly by differences among the Celtic, Mediterranean and Basque breed groups, rather than by differences between domestic and wild pigs. Breeds clustered closely according to group, and proximity was detected between wild pigs and the Mediterranean cluster of breeds. Most breeds had their own structure and identity, with very little evidence of admixture, except for the Retinto and Entrepelado varieties of the Mediterranean group, which are very similar. Genetic influence of the identified breed clusters extends beyond the specific geographical areas across borders throughout the Iberian Peninsula, with a very sharp transition from one breed group to another. Analysis of conservation priorities confirms that the ranking of a breed for conservation depends on the emphasis placed on its contribution to the betweenand within-breed components of genetic diversity. Conclusions: Native pig breeds in Iberia reveal high levels of genetic diversity, a solid breed structure and a clear organization in well-defined clusters.