Changes in trophic state and aquatic communities in high Arctic ponds in response to increasing goose populations

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Effects of exotic <Emphasis Type="Italic">Spartina alterniflora</Emphasis> on the habitat patch associations of breeding saltmarsh birds at Chongming Dongtan in the Yangtze River estuary,China

Smooth cordgrass (Spartina alterniflora) is one of the most invasive exotic plants of saltmarshes worldwide. To understand the effects of smooth cordgrass invasion on the habitat use and selection by breeding saltmarsh birds, we compared species number and abundance of breeding birds in native reed (Phragmites australis) and smooth cordgrass-invaded habitats (reed-cordgrass mixed habitats and cordgrass monocultures) at Chongming Dongtan in the Yangtze River estuary, China. We further examined the similarity of bird communities in different habitats and habitat selection by dominant bird species. For saltmarsh generalists, species number and abundance did not differ among the habitats. For saltmarsh specialists, species number and abundance did not differ in reed monocultures and reed-cordgrass mixed habitats but were significantly lower in cordgrass monocultures than in reed monocultures and reed-cordgrass mixed habitats. ANOSIM indicated that the difference in bird communities was larger between cordgrass monocultures and the habitats with reed than between the habitats with reed. The saltmarsh specialists preferred reed monocultures, while saltmarsh generalists avoided reed monocultures. Most species indicated no selection (neither preferred nor avoided) on reed-cordgrass mixed habitats, and no species preferred the cordgrass monocultures. The use of cordgrass monocultures by the common saltmarsh birds was negatively related to their body size. This study suggests that the spread of exotic smooth cordgrass has greatly affected the species composition and structure of local bird communities and has been especially disadvantageous to the saltmarsh specialists.     

Barrier spraying to control the malaria vector Anopheles albimanus: laboratory and field evaluation in the Dominican Republic

Abstract. To develop a new strategy for control of exophilic/exophagic malaria vectors which rest on peridomestic foliage, Anopheles albimanus was used for laboratory bioassays of mosquito adulticides applied to various vegetation types. Of the three classes of insecticide tested, the pyrethroid (permethrin at 112 g/ha) showed greater foliar persistence than either the carbamate (bendiocarb at 340g/ha) or the organophosphorus compound (malathion at 277g/ha). Field evaluation of barrier spraying against An.albimanus was evaluated in rural villages of southwest Dominican Republic during 1989. The pyrethroid deltamethrin was sprayed aerially for ultra-low volume application at treatment rates of 17-19ga.i./ha in a radius of 500m around two villages. An.albimanus were monitored by light-traps and human bait collections at both treated villages, compared with two similar untreated villages, up to 9 nights post-treatment. Densities of female An.albimanus were significantly reduced in the sprayed villages for at least 8 or 9 nights. Further evaluation of barrier spraying is recommended to determine optimal pyrethroid formulations and applications rates, their impact on non-target fauna and efficacy against malaria transmission.     

Effects of methoprene and Bti (Bacillus thuringiensis var. israelenis) on non-target insects

The effects of mosquito larvicides Bacillus thuringiensis israelensis (Bti) and methoprene, on non-target benthic invertebrates were studied in a divided pond experiment in south-central Minnesota, USA, during the spring and summer of 1989. Density and biomass of insects and other benthic macroinvertebrates were quite low in all sections of the three ponds studied, which may have been due to three consecutive years of drought, but richness appeared to be high and we observed no evidence of dominance by a particular group. We also saw no evidence of negative effects of larvicide treatment on density or biomass of any invertebrate group, nor was there a treatment-related decrease in richness of benthic invertebrate taxa under these drought conditions.     

Production of the bioinsecticide Bacillus thuringiensis subsp. israelensis with deltamethrin increases toxicity towards mosquito larvae

Bacillus thuringiensis subsp. israelensis is a bioinsecticide used for larval mosquito control and it represents a safe alternative to chemical insecticides. Despite its environmental safety, it is less efficient and persistent than chemical insecticides. To bypass these limitations, we propose to combine the advantages of chemical and biological insecticides by producing Bti in a medium supplemented with a chemical insecticide (DDT, deltamethrin, permethrin, propoxur or temephos). Among the investigated insecticides, the addition of deltamethrin in the medium induced a higher toxicity (over 6·72‐fold) of the composite deltamethrin‐Bti towards mosquito larvae as compared to Bti alone. This was mainly due to the insertion of deltamethrin into the membranes of Bti spores, as evidenced by a quantification of membrane‐extracted deltamethrin by HPLC. This composite larvicide is a promising tool to decrease the quantity of chemicals dispersed in the environment, to increase the efficacy of Bti and to facilitate its widespread use as a transition between chemical and biological insecticides. Further experiments are required to characterize the mechanisms that underline the incorporation of deltamethrin into Bti to optimize the production and the toxicity of this composite larvicide.

Significance and Impact of the Study

This study is the first report of an increased efficacy of the mosquitocidal bioinsecticide Bacillus thuringiensis subsp. israelensis (Bti) when produced with a chemical insecticide. The results clearly demonstrate that deltamethrin is able to synergize the insecticidal activity of Bti through inclusion into spore membranes, reducing off‐target and nonspecific toxicity occurring when the chemical is used alone as sprays. This new composite chemical–biological insecticide can become an invaluable tool as an intermediate between single chemical usage and the widespread use of Bti, notably in developing countries with limited financial resources for intensive mosquito control campaigns.     

Field evidence of dispersal of branchiopods, ostracods and bryozoans by teal (Anas?crecca) in the Camargue (southern France)

Invertebrate propagules may survive internal and external transports by waterbirds, thus facilitating their dispersal between aquatic habitats. However, field data on such transport remain limited, especially for exozoochory. We quantified and compared the rates of internal and external invertebrate transports simultaneously in a wintering population of teal (Anas crecca) in the Camargue (southern France). We inspected lower gut (rectum) contents of birds that had been shot (N = 366) and washed birds that had been live-trapped (N = 68) during the winters 2006–2007 and 2007–2008. At least one propagule was recorded in 2.5% and 10.3% of internal and external samples, respectively. Cladoceran, ostracod, plumatellid bryozoan and anostracan propagules were all recorded in both internal and external samples. Hatching confirmed their viability, except for anostracan eggs. At least three cladoceran species and two ostracod species were recorded, none of which had previously been shown to be dispersed by birds. Amongst external samples, we recorded a significant seasonal trend in 1 year with most propagules recorded before December, keeping with a seasonal decline in the availability of propagules on the water surface. This study provides evidence that teal may be important vectors of invertebrate dispersal both within the Camargue and along migratory flyways.     

Seasonal Abundance and Species Richness of Birds in Common Reed Habitats in Lake Erie

Abstract: Common reed (Phragmites australis) forms dense stands with deep layers of residual organic matter that negatively affects plant diversity and possibly habitat use by wetland birds. We sought to determine whether seasonal relative abundance and species richness of birds varied among 3 habitat types in Great Lakes coastal wetland complexes recently invaded by common reed. We used fixed-distance point counts to determine species relative abundances and species richness in edge and interior locales within common reed, cattail (Typha spp.), and meadow marsh habitats of various sizes during 2 summers (2001 and 2002) and 1 autumn (2001) at Long Point, Lake Erie, Ontario, Canada. We found that total relative abundance and species richness of birds were greater in common reed habitat compared to cattail or meadow marsh habitats. However, we also found that relative abundance of marsh-nesting birds was greater in meadow marsh habitat than in cattail and common reed during summer. Lastly, we found that, irrespective of habitat type, habitat edges had higher total relative abundance and species richness of birds than did habitat interiors. Our results show that common reed provides suitable habitat for a diversity of landbirds during summer and autumn but only limited habitat for many marsh-nesting birds during summer. Based on these results, we recommend restoration of meadow marsh habitat through reduction of common reed in Great Lakes wetlands where providing habitat for breeding marsh-nesting birds is an objective. Managers also might consider reducing the size of nonnative common reed stands to increase edge effect and use by birds, possibly including wetland birds.     

Wintering bird communities in newly-formed wetland in the Yangtze River estuary

We compared wintering bird communities and their habitats among three shoals at Jiuduansha, a newly-formed wetland in the Yangtze River estuary. The highest species richness and diversity were recorded in Shangsha, which is the highest shoal, and the highest abundance and lowest species diversity were recorded in Xiasha, which is the lowest shoal. Shangsha had the largest abundance of perching birds whereas Xiasha was the most abundant in waterbirds. Bird assemblages showed different associations with the different habitat types—perching birds were favored by reed (Phragmites australis) communities, shallow water foragers and dabbling ducks preferred sea-bulrush (Scirpus mariqueter) communities, and moist-soil foragers and gulls showed a preference for bare intertidal zones. All bird assemblages, however, avoided the smooth cordgrass (Spartina alterniflora) communities, which are dominated by an alien invasive plant. The composition of avian communities was related to habitat types at the three shoals. Our results suggest that the newly-formed tidelands can provide suitable habitats for waterbirds and that the lower tidelands can attract more waterfowl than the higher tidelands. Because the shoal with low species diversity could have exclusive bird species, conservation efforts should not concentrate only on the area with high species diversity. The estuarine wetlands should be considered as a whole when conservation strategies are designed. The alien invasive plant should, moreover, be effectively controlled, to provide suitable habitats for birds.     

Invertebrate communities associated with macrophytes in Lake Ladoga: effects of environmental factors

Littoral invertebrate communities (meio- and macrobenthos and zooplankton) were studied in seven types of macrophyte associations commonly encountered in Lake Ladoga: in reed (Phragmites) beds on sand, soft and hard bottoms, in associations with the prevalence of Potamogeton spp., Carex spp., and Equisetum fluviatile, and in diverse vegetation stands with e.g. Polygonum amphibium, Cicuta virosa, Typha latifolia and Eleocharis acicularis. Some of the studied habitats were affected by sewage pollution, others were in comparatively undisturbed areas. Statistically significant differences between invertebrate communities in the different macrophyte associations were found. In stepwise multiple linear regression analysis the following factors were identified as determinants of abundance of aquatic invertebrates in macrophyte associations: shoot density, plant dry weight biomass, periphyton biomass, periphyton chlorophyll a, periphyton primary production, and concentrations of Sr, Mg, Ca, P, Mn, Zn, Pb and Cu. Pollution was shown to have a minor effect on the composition of littoral invertebrate communities. It is not possible to determine one single principle factor responsible for the structure and density of invertebrates in macrophyte communities.     

Top–down control by great blue herons Ardea herodias regulates seagrass‐associated epifauna

Top predators can influence the structure and function of plant and animal communities. In coastal marine systems, fish, shark and mammal population declines are major drivers of recent ecosystem‐level change. Cascading effects of predatory wading birds, however, are less understood, even though wading bird populations have declined in many regions. We quantified the effects of predation by the piscivorous great blue heron Ardea herodias fannini on fish, invertebrates and epiphytes living in eelgrass Zostera marina. We found that herons forage on benthic fish in seagrass meadows, and foraging intensity increased from late spring until midsummer. When we experimentally excluded herons, benthic fish abundance increased, and the invertebrate assemblage shifted to more shrimp‐dominated assemblages while grazing gammarid amphipod abundance declined. These shifts were associated with reduced epiphyte abundance when herons were excluded, reflecting a four‐level trophic cascade and mediated by shifts in the grazer assemblage. In summary, we found that a piscivorous wading bird species exerts top down control in a subtidal seagrass ecosystem. Losses and recovery of wading birds could have ecosystem‐level ecological consequences that may need to be considered in the context of concern for overfishing and predator recovery in marine coastal management.     

Influence of competing and predatory invertebrate taxa on larval populations of mosquitoes in temporary ponds of wetland areas in Germany

Abundances of mosquito larvae and associated invertebrate communities were assessed in 27 temporary ponds during the spring season in wetland areas of Germany. Four genera of mosquitoes were identified: Aedes, Anopheles, Culex, and Culiseta. We focused our analyses on Aedes spp. because this genus was the most abundant (92% of total abundance) and frequently encountered mosquito (present in 65% of investigated sites). The abundance of Aedes spp. was negatively associated with the abundance of competitors for food, and to a lesser extent with those of intraguild predators and strict predators. The influence of these natural antagonists on larvae of Aedes was stronger in ponds with higher levels of dissolved oxygen (53 ± 4%) than in ponds with lower levels (16 ± 1%). The overall abundance of antagonists explained 42% of the variation in abundance of Aedes spp. at sites with higher levels of dissolved oxygen. Of this explained variation, competitors accounted for 34.7%, whereas the abundance of intraguild predators and strict predators accounted for only 6.8 and 0.5%, respectively. Therefore, the promotion of competing species might be an appropriate ecological approach for the control of Aedes spp. in temporary ponds in these areas.     

Genome scan in the mosquito Aedes rusticus: population structure and detection of positive selection after insecticide treatment

Identification of genes involved in local adaptation is particularly challenging for species functioning as a network of interconnected populations undergoing frequent extinctions–recolonizations, because populations are submitted to contrasted evolutionary pressures. Using amplified fragment length polymorphism markers, population genetic structure of the mosquito Aedes rusticus was analysed in five geographical areas of the French Rhône‐Alpes region. We included a number of sites that were treated with the bio‐insecticide Bacillus thuringiensis israelensis (Bti) for more than 15 years. Analysis of molecular variance revealed that most of the genetic variability was found within populations (96%), with no significant variation among geographical areas, although variation among populations within areas (4%) was significant. The global genetic differentiation index F_ST was low (0.0366 ± 0.167). However, pairwise F_ST values were significant and no isolation‐by‐distance at the regional level was observed, suggesting a metapopulation structure in this species. Bti‐treatment had no effect on genetic structure and on within‐population genetic diversity. Potential signatures of positive selection associated with Bti‐treatment were detected for five loci, even though toxicological bioassays performed on field‐collected larvae showed no significant difference in mortality between Bti‐treated and nontreated sites. The difficulty of detecting moderate resistance in field‐collected larvae together with possible differential persistence of toxins in the environment may explain our inability to detect a toxicological response to Bti in treated sites. The evidence for positive selection occurring at several genomic regions suggests a first step towards Bti resistance in natural mosquito populations treated with this bio‐insecticide. Furthermore, this signal was detectable using genomic tools before any toxicological evidence for resistance could be identified.     

Bird abundance and species richness on Florida lakes: influence of trophic status,lake morphology,and aquatic macrophytes

Data from 46 Florida lakes were used to examine relationships between bird abundance (numbers and biomass) and species richness, and lake trophic status, lake morphology and aquatic macrophyte abundance. Average annual bird numbers ranged from 7 to 800 birds km^–2 and bird biomass ranged from 1 to 465 kg km^–2. Total species richness ranged from 1 to 30 species per lake. Annual average bird numbers and biomass were positively correlated to lake trophic status as assessed by total phosphorus (r = 0.61), total nitrogen (r = 0.60) and chlorophyll a (r = 0.56) concentrations. Species richness was positively correlated to lake area (r = 0.86) and trophic status (r = 0.64 for total phosphorus concentrations). The percentage of the total annual phosphorus load contributed to 14 Florida lakes by bird populations was low averaging 2.4%. Bird populations using Florida lakes, therefore, do not significantly impact the trophic status of the lakes under natural situations, but lake trophic status is a major factor influencing bird abundance and species richness on lakes. Bird abundance and species richness were not significantly correlated to other lake morphology or aquatic macrophyte parameters after the effects of lake area and trophic status were accounted for using stepwise multiple regression. The lack of significant relations between annual average bird abundance and species richness and macrophyte abundance seems to be related to changes in bird species composition. Bird abundance and species richness remain relatively stable as macrophyte abundance increases, but birds that use open-water habitats (e.g., double-crested cormorant, Phalacrocorax auritus) are replaced by species that use macrophyte communities (e.g., ring-necked duck, Aythya collaris).     

Impacts of cadmium contamination and fish presence on wetland invertebrate communities: An application of population measures and multi-metric tests

Wetlands are extensively used in heavy metal bioremediation, and it is important to know how biota are impacted by such toxins. I examined invertebrate communities in six experimental wetland ponds in Ithaca, NY, USA to assess the effects of residual cadmium. Three ponds had been treated with cadmium in 1983, and still had average levels of 3.6 mg/kg in the sediment in 2001. Also, two of the cadmium ponds and one non-cadmium pond had predatory fish populations. I quantified the variable effects on invertebrate communities using non-parametric statistics, CCA (canonical correspondence analysis), and three published multi-metric tests (Burton et al., 1999, Apfelbeck, 2001, Helgen and Gernes, 2001). Cadmium effects could not be seen in ponds with fish because invertebrate abundance in these ponds was low. In ponds without fish, cadmium appeared to have significant influence on invertebrate abundance, but not on diversity. None of the multi-metric tests detected a cadmium impact. This study suggests that trophic interactions between fish and invertebrates should be considered in wetland index development and implementation.     

Monitoring resistance to Bacillus thuringiensis subsp. israelensis in the field by performing bioassays with each Cry toxin separately

Bacillus thuringiensis subsp. israelensis (Bti) is increasingly used worldwide for mosquito control and is the only larvicide used in the French Rhône-Alpes region since decades. The artificial selection of mosquitoes with field-persistent Bti collected in breeding sites from this region led to a moderate level of resistance to Bti, but to relatively high levels of resistance to individual Bti Cry toxins. Based on this observation, we developed a bioassay procedure using each Bti Cry toxin separately to detect cryptic Bti-resistance evolving in field mosquito populations. Although no resistance to Bti was detected in none of the three mosquito species tested (Aedes rusticus, Aedes sticticus and Aedes vexans), an increased tolerance to Cry4Aa (3.5-fold) and Cry11Aa toxins (8-fold) was found in one Ae. sticticus population compared to other populations of the same species, suggesting that resistance to Bti may be arising in this population. This study confirms previous works showing a lack of Bti resistance in field mosquito populations treated for decades with this bioinsecticide. It also provides a first panorama of their susceptibility status to individual Bti Cry toxins. In combination with bioassays with Bti, bioassays with separate Cry toxins allow a more sensitive monitoring of Bti-resistance in the field.     

The efficacy of high and low volume spray applications of Mimic® (tebufenozide) for managing autumn gum moth larvae Mnesampela privata (Lepidoptera: Geometridae) in eucalypt plantations

Abstract 1 The autumn gum moth Mnesampela privata (Guenée) (Lepidoptera: Geometridae, Ennominae) is a native moth that can outbreak, resulting in significant defoliation of plantation eucalypts in southern Australia. 2 Laboratory trials tested M. privata larvae for their dose–response to the ecdysone agonist, Mimic® 700 WP (a.i. 700 g/kg tebufenozide); ground and aerial field trials also tested its efficacy in eucalypt plantations. 3 The laboratory trials showed that there was no significant difference in mortality between larvae treated with 172 g Mimic® (120 g a.i)/ha and those sprayed with doses ranging from 86 to 3340 g Mimic®/ha. 4 Laboratory and field trials demonstrated that second instars were the most susceptible, with the most rapid response. However, second to fourth instars all reached 100% and fifth instars 90% mortality 3 weeks after aerial spraying at 120 g a.i./ha. 5 Aerial spraying an Eucalyptus globulus plantation with 120 g a.i. Mimic® at 20 L/ha caused 95% mortality of instars two to five, and 100% for instars two to four within 3 weeks after spraying. 6 Ground spraying to run‐off with 120 g a.i. Mimic®/ha reduced defoliation of E. grandis from between 67% to 80% for unsprayed trees to 0% defoliation for sprayed trees. 7 The window for effective management of M. privata larvae is 3–5 weeks, during first to third instar development. 8 Replacement of broad‐spectrum insecticides with the more target‐specific Mimic® should increase the biodiversity of plantations and therefore would be more environmentally friendly.     

Seasonal dynamics in mosquito abundance and temperature do not influence avian malaria prevalence in the Himalayan foothills

We examined seasonal prevalence in avian haemosporidians (Plasmodium and Haemoproteus) in migrant and resident birds in western Himalaya, India. We investigated how infection with haemosporidians in avian hosts is associated with temporal changes in temperature and mosquito abundance along with host abundance and life‐history traits (body mass). Using molecular methods for parasite detection and sequencing partial cytochrome b gene, 12 Plasmodium and 27 Haemoproteus lineages were isolated. Our 1‐year study from December 2008 to December 2009 in tropical Himalayan foothills revealed a lack of seasonal variation in Plasmodium spp. prevalence in birds despite a strong correlation between mosquito abundance and temperature. The probability of infection with Plasmodium decreased with increase in temperature. Total parasite prevalence and specifically Plasmodium prevalence showed an increase with average avian body mass. In addition, total prevalence exhibited a U‐shaped relationship with avian host abundance. There was no difference in prevalence of Plasmodium spp. or Haemoproteus spp. across altitudes; parasite prevalence in high‐altitude locations was mainly driven by the seasonal migrants. One Haemoproteus lineage showed cross‐species infections between migrant and resident birds. This is the first molecular study in the tropical Himalayan bird community that emphasizes the importance of studying seasonal variation in parasite prevalence. Our study provides a basis for further evolutionary study on the epidemiology of avian malaria and spread of disease across Himalayan bird communities, which may not have been exposed to vectors and parasites throughout the year, with consequential implications to the risk of infection to naïve resident birds in high altitude.     

How do local differences in saltmarsh ecology influence disease vector mosquito populations?

Saltmarsh breeding mosquitoes are an important source of vectors for arboviral transmission. In southern Australia, the most prominent vector borne disease, Ross River virus (Togaviridae: Alphavirus) (RRV), is transmitted by the saltmarsh mosquito (Diptera: Culicidae) Aedes camptorhynchus (Thomson). However, the factors driving the abundance of this mosquito within and among saltmarshes are poorly understood. To predict the abundance of this mosquito within saltmarshes, the environmental conditions and aquatic invertebrate ecology of three temperate saltmarshes habitats were monitored over two seasons. Up to 44% of first-instar mosquito numbers and 21% of pupal numbers were accounted for by environmental variables. Samphire vegetation cover was a common predictor of first-instar numbers across sites although, between saltmarshes, aquatic factors such as high salinity, temperatures less than 22 °C and water body volume were important predictors. The identified predictors of pupal numbers were more variable and included high tides, waterbody volume and alkalinity. The composition of invertebrate functional feeding groups differed between saltmarshes and showed that an increased diversity led to fewer mosquitoes. It was evident that apparently similar saltmarshes can vary markedly in invertebrate assemblages, water availability and conditions through tidal inundations, rainfall or waterbody permanency. The present study advances insight into predictors of vector mosquito numbers that drive the risk of RRV outbreaks.     

Transstadial Effects of Bti on Traits of Aedes aegypti and Infection with Dengue Virus

Most mosquito control efforts are primarily focused on reducing the adult population size mediated by reductions in the larval population, which should lower risk of disease transmission. Although the aim of larviciding is to reduce larval abundance and thus recruitment of adults, nonlethal effects on adults are possible, including transstadial effects on phenotypes of adults such as survival and pathogen infection and transmission. In addition, the mortality induced by control efforts may act in conjunction with other sources of mosquito mortality in nature. The consequences of these effects and interactions may alter the potential of the population to transmit pathogens. We tested experimentally the combined effects of a larvicide (Bacillus thuringiensis ssp. israelensis, Bti) and competition during the larval stages on subsequent Aedes aegypti (Linnaeus) traits, population performance, and susceptibility to dengue-1 virus infection. Ae. aegypti that survived exposure to Bti experienced accelerated development, were larger, and produced more eggs with increasing amounts of Bti, consistent with competitive release among surviving mosquitoes. Changing larval density had no significant interactive effect with Bti treatment on development and growth to adulthood. Larval density, but not Bti or treatment interaction, had a strong effect on survival of adult Ae. aegypti females. There were sharper declines in cumulative daily survival of adults from crowded than uncrowded larval conditions, suggesting that high competition conditions of larvae may be an impediment to transmission of dengue viruses. Rates of infection and dengue-1 virus disseminated infections were found to be 87±13% and 88±12%, respectively. There were no significant treatment effects on infection measurements. Our findings suggest that larvicide campaigns using Bti may reduce the number of emerged adults, but survivors will have a fitness advantage (growth, development, enhanced production of eggs) relative to conspecifics that are not under larvicide pressure. However, under most circumstances, these transstadial effects are unlikely to outweigh reductions in the adult population by Bti and altered risk of disease transmission.     

Reverse latitudinal trends in species richness of pitcher-plant food webs

Latitudinal patterns in species richness have been well documented for guilds and individual trophic groups, but comparable patterns for entire, multitrophic communities have not been described. We studied the entire food web that inhabits the water‐filled leaves of the pitcher plant Sarracenia purpurea across North America at two spatial scales: among sites and among leaves within sites. Contrary to the expectation, total species richness at both scales increased with latitude, because of increasing species richness at the lower trophic levels. This latitudinal pattern may be driven by a top‐down effect. The abundance of the mosquito Wyeomyia smithii, a ubiquitous top predator in this system, decreases from south to north and may permit greater species richness of prey trophic levels at higher latitudes.