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AB - Abstract Abundance of sarcosaprophagous Calyptratae species was monitored by using baited traps and active captures with hand net. Analysis of field data collected in three protected areas in the Valdivian temperate forest of South America (Lanín National Park, Lago Puelo National Park, and Los Alerces National Park) indicated that bottle traps baited with putrescine is a reliable method to estimate local abundance of sarcosaprophagous species by comparison to the active capture method. Also, we describe and compare general patterns of sex bias for four dominant species: Sarconesia magellanica (Le Guillou), Calliphora vicina Robineau-Desvoidy, Microcerella spinigena (Rondani), and Oxysarcodexia varia (Walker). From these analyses, it can be concluded that abundance fluctuations of flies showed significant relationship between the sampling methods. This study showed that besides the expected interspecific differences in trapping efficiency, there are acute intraspecific differences of sex ratios between sampling methods. sarcosaprophagous, Diptera, Calyptratae, sampling method Patchy and ephemeral nutrient-rich resources, as carrion or dung, are usually exploited by wide variety of Diptera. Among the most species-rich infraorders of Diptera, Calyptratae include a rich subset of species whose larvae are scavengers or dung feeders, usually included within the so-called sarcosaprophagous guild and thus involved in organic matter decomposition (Yeates et al. 2007, Brown et al. 2009, Marshall 2012). Taking into account their life cycle, great dispersal ability, and elusive flying behavior to catch them directly, the most frequent method for monitoring sarcosaprophagous flies in wild environments is through the use of olfactory stimuli with baits of attraction. Thus, the use of organic matter as baits placed inside a trapping device is widely used to attract adult Diptera for ecological or taxonomic samples (Hall 1995, Centeno et al. 2004, Baz et al. 2007, Greco et al. 2014). In such circumstances, the baited traps emit an odor to produce the aggregation of these very mobile insects that enter the diffusion range of the odor, thus the capture of insects will not be random. Despite their wide use, field validations of bait performance are usually not assessed in comparison to other sampling methods (especially those that not affect fly behavior) when monitoring programs are designed. When baits are used, biased samples are unavoidable as the trapping method involves different inherent behavioral responses of the species under study to the trap stimulus. Such methods are, however, valuable for making relative comparisons between sites and easy to apply in replicated samples (Hwang and Turner 2005). On the other hand, a generalized collecting technique among entomologists is the active capture method, in which all specimens found in the field are captured directly by the researcher with an entomological net when insects are sighted foraging on flowers or leaves, resting on soil or stones, or in flight. In contrast to baited traps, active capture might be theoretically a potential useful tool to analyze the use of habitat types or natural resting places of different species, as it does not imply an ‘induced’ concentration of specimens from surrounding areas due to the bait effect and does not affect species behavior derived from the attractants. However, the active capture method is fundamentally a collector-dependent method (depending on his ability and expertise to capture flies, or particular interest toward certain specific taxa) and not easily replicable. In any case, the application of adequate sampling methodology is crucial for the exploration of insect abundance or other ecological traits (e.g., dispersal habits, differential resource use, etc.; Olea et al. 2017). The baited trap and active capture techniques involve well-differentiated capture mechanisms and are exposed to different factors that affect their efficiency, or imply particular capture biases. One of the main effects associated with the use of baited traps is that their attractiveness can be different for males and females of different species (Muirhead-Thomson 1968). In addition, the detection of sex ratio phenotypes of a given species is typically obtained by measures of the number of males and females captured in natural populations. However, the adult sex ratio is influenced by the primary sex ratio and also by several other factors (e.g., sex differences in time of emergence, age at maturation, reproductive life span, differential survival, mating behavior, differential resource use, or migration patterns; Hardy 2002). Assessing how the data on catches frequency and sex ratio of sarcosaprophagous Calyptratae can be sensitive to sampling methodology should be of value to both basic and forensic researchers. Indeed, few studies have concentrated on the reliability of trapping data for the assessment of life-history aspects, such as local abundance, sex ratio, or behavioral traits of species. The aim of this work is to compare the captures of sarcosaprophagous flies by these two well-differentiated distinct mechanisms of sampling, baited traps and active capture, occurring for species of sarcosaprophagous Calyptratae inhabiting the Valdivian temperate forest of South America. Also, to describe and compare general patterns of sex bias for the species, according to the method employed. Thus, specifically goals of this work were to assess the performance of traps baited with putrecine as a reliable method to estimate local abundance of sarcosaprophagous species in comparison to active capture samplings. Materials and Methods Study Site and Collecting Methods Sampling sites were distributed in Lanín National Park (LNP), Lago Puelo National Park (LPNP), and Los Alerces National Park (LANP) that are located in Neuquén and Chubut provinces, respectively, Argentina (Fig. 1). Samplings were performed during the late spring and summer, which represents a warmer and dry season, the period of highest abundance of flies for the region. Fig. 1. View largeDownload slide Map of Valdivian temperate forests of South America (green), with the three study areas (orange), Lanín National Park (LNP), Lago Puelo National Park (LPNP), and Los Alerces National Park (LANP). Fig. 1. View largeDownload slide Map of Valdivian temperate forests of South America (green), with the three study areas (orange), Lanín National Park (LNP), Lago Puelo National Park (LPNP), and Los Alerces National Park (LANP). Seven collecting campaigns (i.e., area by year) were considered for the analyses; each represents a single independent observation of sex ratio and capture rate of the species. The seven campaign carried out have covered the LPNP and LANP during two consecutive warm seasons and three different areas of the extensive LNP (northern, central, and southern areas). Each campaign includes three to four sampling sites. The sampling effort of each collecting campaign is summarized in Table 1. Table 1. Baited traps and active captures distributed in LANP, LNP, and LPNP, Argentina Location (date) Georreference Baited traps Active captures LPNP (Jan-2011) 24 24  Pitranto Grande −42.0963, −71.6129 6 6  Los Hitos −42.1047, −71.7262 6 6  Río Turbio −42.2280, −71.6675 6 6  Rio Azul 1 −42.0927, −71.6286 6 6 LPNP (Jan-2012) 16 16  Gendarmería 1 −42.0973, −71.6821 4 4  La Playita −42.0974, −71.6155 4 4  Gendarmería 2 −42.0994, −71.6845 4 4  Río Azul 2 −42.0910, −71.6275 4 4 LNP, southern area (Feb-2011) 24 24  Hua Hum −40.1153, −71.6606 6 6  Mirador Bandurrias −40.1630, −71.3684 6 6  Seccional Bandurrias −40.1455, −71.3468 6 6  Laguna Pudú Pudú −40.3620, −71.4749 6 6 LNP, northern area (Jan-2013) 27 18  Ñorquinco −39.1512, −71.2563 9 6  Rucachoroi −39.2314, −71.1773 9 6  Quillen −39.3613, −71.2188 9 6 LNP, central area (Dec-2013) 27 18  Huechulafquen −39.7891, −71.2193 9 6  Arroyo Los Pinos −39.8794, −71.4559 9 6  Paso Tromen −39.5875, −71.4313 9 6 LANP (Feb-2013) 27 18  Cabaña La Cascada −42.8886, −71.5927 9 6  Lago Futalaufquen −42.8847, −71.5999 9 6  Río Stange −42.8725, −71.7736 9 6 LANP (Oct-2014) 27 18  Lago Verde −42.7188, −71.7274 9 6  Puerto Mermoud −42.72319, −71.7488 9 6  Arroyo Torcido −42.7613, −71.7506 9 6 Location (date) Georreference Baited traps Active captures LPNP (Jan-2011) 24 24  Pitranto Grande −42.0963, −71.6129 6 6  Los Hitos −42.1047, −71.7262 6 6  Río Turbio −42.2280, −71.6675 6 6  Rio Azul 1 −42.0927, −71.6286 6 6 LPNP (Jan-2012) 16 16  Gendarmería 1 −42.0973, −71.6821 4 4  La Playita −42.0974, −71.6155 4 4  Gendarmería 2 −42.0994, −71.6845 4 4  Río Azul 2 −42.0910, −71.6275 4 4 LNP, southern area (Feb-2011) 24 24  Hua Hum −40.1153, −71.6606 6 6  Mirador Bandurrias −40.1630, −71.3684 6 6  Seccional Bandurrias −40.1455, −71.3468 6 6  Laguna Pudú Pudú −40.3620, −71.4749 6 6 LNP, northern area (Jan-2013) 27 18  Ñorquinco −39.1512, −71.2563 9 6  Rucachoroi −39.2314, −71.1773 9 6  Quillen −39.3613, −71.2188 9 6 LNP, central area (Dec-2013) 27 18  Huechulafquen −39.7891, −71.2193 9 6  Arroyo Los Pinos −39.8794, −71.4559 9 6  Paso Tromen −39.5875, −71.4313 9 6 LANP (Feb-2013) 27 18  Cabaña La Cascada −42.8886, −71.5927 9 6  Lago Futalaufquen −42.8847, −71.5999 9 6  Río Stange −42.8725, −71.7736 9 6 LANP (Oct-2014) 27 18  Lago Verde −42.7188, −71.7274 9 6  Puerto Mermoud −42.72319, −71.7488 9 6  Arroyo Torcido −42.7613, −71.7506 9 6 View Large Table 1. Baited traps and active captures distributed in LANP, LNP, and LPNP, Argentina Location (date) Georreference Baited traps Active captures LPNP (Jan-2011) 24 24  Pitranto Grande −42.0963, −71.6129 6 6  Los Hitos −42.1047, −71.7262 6 6  Río Turbio −42.2280, −71.6675 6 6  Rio Azul 1 −42.0927, −71.6286 6 6 LPNP (Jan-2012) 16 16  Gendarmería 1 −42.0973, −71.6821 4 4  La Playita −42.0974, −71.6155 4 4  Gendarmería 2 −42.0994, −71.6845 4 4  Río Azul 2 −42.0910, −71.6275 4 4 LNP, southern area (Feb-2011) 24 24  Hua Hum −40.1153, −71.6606 6 6  Mirador Bandurrias −40.1630, −71.3684 6 6  Seccional Bandurrias −40.1455, −71.3468 6 6  Laguna Pudú Pudú −40.3620, −71.4749 6 6 LNP, northern area (Jan-2013) 27 18  Ñorquinco −39.1512, −71.2563 9 6  Rucachoroi −39.2314, −71.1773 9 6  Quillen −39.3613, −71.2188 9 6 LNP, central area (Dec-2013) 27 18  Huechulafquen −39.7891, −71.2193 9 6  Arroyo Los Pinos −39.8794, −71.4559 9 6  Paso Tromen −39.5875, −71.4313 9 6 LANP (Feb-2013) 27 18  Cabaña La Cascada −42.8886, −71.5927 9 6  Lago Futalaufquen −42.8847, −71.5999 9 6  Río Stange −42.8725, −71.7736 9 6 LANP (Oct-2014) 27 18  Lago Verde −42.7188, −71.7274 9 6  Puerto Mermoud −42.72319, −71.7488 9 6  Arroyo Torcido −42.7613, −71.7506 9 6 Location (date) Georreference Baited traps Active captures LPNP (Jan-2011) 24 24  Pitranto Grande −42.0963, −71.6129 6 6  Los Hitos −42.1047, −71.7262 6 6  Río Turbio −42.2280, −71.6675 6 6  Rio Azul 1 −42.0927, −71.6286 6 6 LPNP (Jan-2012) 16 16  Gendarmería 1 −42.0973, −71.6821 4 4  La Playita −42.0974, −71.6155 4 4  Gendarmería 2 −42.0994, −71.6845 4 4  Río Azul 2 −42.0910, −71.6275 4 4 LNP, southern area (Feb-2011) 24 24  Hua Hum −40.1153, −71.6606 6 6  Mirador Bandurrias −40.1630, −71.3684 6 6  Seccional Bandurrias −40.1455, −71.3468 6 6  Laguna Pudú Pudú −40.3620, −71.4749 6 6 LNP, northern area (Jan-2013) 27 18  Ñorquinco −39.1512, −71.2563 9 6  Rucachoroi −39.2314, −71.1773 9 6  Quillen −39.3613, −71.2188 9 6 LNP, central area (Dec-2013) 27 18  Huechulafquen −39.7891, −71.2193 9 6  Arroyo Los Pinos −39.8794, −71.4559 9 6  Paso Tromen −39.5875, −71.4313 9 6 LANP (Feb-2013) 27 18  Cabaña La Cascada −42.8886, −71.5927 9 6  Lago Futalaufquen −42.8847, −71.5999 9 6  Río Stange −42.8725, −71.7736 9 6 LANP (Oct-2014) 27 18  Lago Verde −42.7188, −71.7274 9 6  Puerto Mermoud −42.72319, −71.7488 9 6  Arroyo Torcido −42.7613, −71.7506 9 6 View Large Baited traps consisted of a modification of the bottle trap used by Hwang and Turner (2005). These traps have at their base a plastic jar measuring approximately 150 mm in diameter and 200 mm in height. They have four lateral openings (2 × 2 cm) and a funnel in their upper part, manufactured with a plastic bottle, which allows the entry of dipterous insects but blocks their way out, through another bottle placed above. In the interior of the plastic jar, there is a container covered by a piece of Lycra, where the bait is placed. The bait used in the traps was bone meal (putrescine), which is a foul-smelling organic chemical compound produced by the breakdown of amino acids in living and dead organisms. These baited traps were placed in all selected sites of both national parks at 10:00 a.m. and extracted at approximately 04:00 p.m. This range covers the period of highest activity of the flies. The active capture method involves the capture of all specimens encountered using an entomological net while foraging on flowers or vegetation, resting on soil or stones, or in flight. These captures took place in areas adjacent to those sites where the baited traps were placed but keeping separated at least by 50 m. These captures were done for 2 h by three researchers at each location sampled. Species Selected To accomplish the goals of the study, we selected five sarcosaprophagous species following a dominance criterion. Thus, we targeted the study to the most abundant species of the sacrosaprophagous community to obtain comparative data in both sampling methods. Taxonomic identifications were performed using specialized literature of local fauna: Calliphoridae (Mariluis and Schnack 2002), Muscidae (Huckett 1954), and Sarcophagidae (Hall 1937, Mulieri et al. 2015b). The species analyzed were Sarconesia magellanica (Le Guillou, 1842), Calliphora vicina Robineau-Desvoidy, 1830, Compsomyiops fulvicrura (Walker, 1830), among Calliphoridae; Oxysarcodexia varia (Walker, 1836) and Microcerella spinigena (Rondani, 1864) among Sarcophagidae; and a single muscid species, Hydrotaea acuta Stein, 1898 (Muscidae). Voucher specimens of these taxa are housed in the Museo Argentino de Ciencias Naturales ‘Bernardino Rivadavia’, Buenos Aires, Argentina. Capture Rate Frequency of capture was compared between methods. To perform this analysis, the number of specimens collected was standardized taking into account the number of flies per hour per sample unit for each sampling method (capture rate = CR). A T-test for two dependent samples (Zar 1996) was applied to analyze whether there were differences in capture rates between the different methods. Linear regression analyses were used to investigate the relationships between capture rates obtained by both sampling methods (Zar 1996). For this analysis, the dependent variable was capture rate of active capture and the independent variable was the capture rate of baited trap for all species analyzed. Sex Ratio The estimator to describe the sex ratio of a species was total proportion of females (Pf; Mulieri et al. 2015a). For the comparison of the sex ratio between sampling methods, we only considered those observations where Pf was based on frequencies of at least 10 individuals caught in a campaign (area by year) for each method. Hence, those cases in which there were no flies, or their number was very low in at least one of the methods, were discarded. Data of Pf was normalized by the arcsine square root transformation. A T-test for two dependent samples was applied to determine whether there were differences in sex ratio between the sampling methods. In addition, linear regression analyses were performed to evaluate the relationships between capture rates of females and males, separately for each method. As baited trap usually produce female-biased samples, we fixed the capture rate of females as independent variable and males as dependent variable. The same criterion was followed for model based on active capture. Results The set of selected species for this study account for the 60% of total captures of sarcosaprophagous Calyptratae obtained on baited traps and active capture. Four species were relatively well represented in both methods (O. varia, M. spinigena, S. magellanica, and C. vicina). In the case of H. acuta and C. fulvicrura, they were almost exclusively obtained by means of baited traps (Table 2). Table 2. Raw frequencies of flies obtained with baited traps and active captures in LANP, LNP, and LPNP, Argentina Species Site (date) Baited trap Active capture ♂ ♀ ♂ ♀ Calliphoridae  Sarconesia magellanica LPNP (Jan-2011) 21 32 7 4 LPNP (Jan-2012) 100 92 9 5 LNP, southern (Feb-2011) 85 59 14 4 LNP, northern (Jan-2013) 9 13 0 0 LNP, central (Dec-2013) 2 1 0 0 LANP (Oct-2014) 49 56 0 3 LANP (Feb-2013) 0 0 0 0  Calliphora vicina LPNP (Jan-2011) 26 37 12 8 LPNP (Jan-2012) 14 26 5 6 LNP, southern (Feb-2011) 14 14 1 1 LNP, northern (Jan-2013) 0 0 0 0 LNP, central (Dec-2013) 1 2 0 1 LANP (Oct-2014) 0 12 0 1 LANP (Feb-2013) 56 72 27 29  Compsomyiops fulvicrura LPNP (Jan-2011) 2 14 3 1 LPNP (Jan-2012) 16 24 1 0 LNP, southern (Feb-2011) 2 4 1 0 LNP, northern (Jan-2013) 8 44 1 0 LNP, central (Dec-2013) 20 29 2 1 LANP (Oct-2014) 0 25 0 1 LANP (Feb-2013) 0 0 0 0 Sarcophagidae  Oxysarcodexia varia LPNP (Jan-2011) 342 88 72 21 LPNP (Jan-2012) 13 31 4 4 LNP, southern (Feb-2011) 15 40 7 6 LNP, northern (Jan-2013) 55 34 20 4 LNP, central (Dec-2013) 38 17 2 4 LANP (Oct-2014) 11 44 6 5 LANP (Feb-2013) 0 0 1 0  Microcerella spinigena LPNP (Jan-2011) 1 7 14 13 LPNP (Jan-2012) 28 23 12 9 LNP, southern (Feb-2011) 1 13 18 14 LNP, northern (Jan-2013) 9 17 20 17 LNP, central (Dec-2013) 8 20 2 2 LANP (Oct-2014) 34 88 36 22 LANP (Feb-2013) 0 1 20 4 Muscidae  Hydrotaea acuta LPNP (Jan-2011) 13 68 1 0 LPNP (Jan-2012) 0 3 0 0 LNP, southern (Feb-2011) 14 80 2 0 LNP, northern (Jan-2013) 6 19 0 0 LNP, central (Dec-2013) 0 4 0 0 LANP (Oct-2014) 1 8 0 0 LANP (Feb-2013) 0 0 0 0 Species Site (date) Baited trap Active capture ♂ ♀ ♂ ♀ Calliphoridae  Sarconesia magellanica LPNP (Jan-2011) 21 32 7 4 LPNP (Jan-2012) 100 92 9 5 LNP, southern (Feb-2011) 85 59 14 4 LNP, northern (Jan-2013) 9 13 0 0 LNP, central (Dec-2013) 2 1 0 0 LANP (Oct-2014) 49 56 0 3 LANP (Feb-2013) 0 0 0 0  Calliphora vicina LPNP (Jan-2011) 26 37 12 8 LPNP (Jan-2012) 14 26 5 6 LNP, southern (Feb-2011) 14 14 1 1 LNP, northern (Jan-2013) 0 0 0 0 LNP, central (Dec-2013) 1 2 0 1 LANP (Oct-2014) 0 12 0 1 LANP (Feb-2013) 56 72 27 29  Compsomyiops fulvicrura LPNP (Jan-2011) 2 14 3 1 LPNP (Jan-2012) 16 24 1 0 LNP, southern (Feb-2011) 2 4 1 0 LNP, northern (Jan-2013) 8 44 1 0 LNP, central (Dec-2013) 20 29 2 1 LANP (Oct-2014) 0 25 0 1 LANP (Feb-2013) 0 0 0 0 Sarcophagidae  Oxysarcodexia varia LPNP (Jan-2011) 342 88 72 21 LPNP (Jan-2012) 13 31 4 4 LNP, southern (Feb-2011) 15 40 7 6 LNP, northern (Jan-2013) 55 34 20 4 LNP, central (Dec-2013) 38 17 2 4 LANP (Oct-2014) 11 44 6 5 LANP (Feb-2013) 0 0 1 0  Microcerella spinigena LPNP (Jan-2011) 1 7 14 13 LPNP (Jan-2012) 28 23 12 9 LNP, southern (Feb-2011) 1 13 18 14 LNP, northern (Jan-2013) 9 17 20 17 LNP, central (Dec-2013) 8 20 2 2 LANP (Oct-2014) 34 88 36 22 LANP (Feb-2013) 0 1 20 4 Muscidae  Hydrotaea acuta LPNP (Jan-2011) 13 68 1 0 LPNP (Jan-2012) 0 3 0 0 LNP, southern (Feb-2011) 14 80 2 0 LNP, northern (Jan-2013) 6 19 0 0 LNP, central (Dec-2013) 0 4 0 0 LANP (Oct-2014) 1 8 0 0 LANP (Feb-2013) 0 0 0 0 View Large Table 2. Raw frequencies of flies obtained with baited traps and active captures in LANP, LNP, and LPNP, Argentina Species Site (date) Baited trap Active capture ♂ ♀ ♂ ♀ Calliphoridae  Sarconesia magellanica LPNP (Jan-2011) 21 32 7 4 LPNP (Jan-2012) 100 92 9 5 LNP, southern (Feb-2011) 85 59 14 4 LNP, northern (Jan-2013) 9 13 0 0 LNP, central (Dec-2013) 2 1 0 0 LANP (Oct-2014) 49 56 0 3 LANP (Feb-2013) 0 0 0 0  Calliphora vicina LPNP (Jan-2011) 26 37 12 8 LPNP (Jan-2012) 14 26 5 6 LNP, southern (Feb-2011) 14 14 1 1 LNP, northern (Jan-2013) 0 0 0 0 LNP, central (Dec-2013) 1 2 0 1 LANP (Oct-2014) 0 12 0 1 LANP (Feb-2013) 56 72 27 29  Compsomyiops fulvicrura LPNP (Jan-2011) 2 14 3 1 LPNP (Jan-2012) 16 24 1 0 LNP, southern (Feb-2011) 2 4 1 0 LNP, northern (Jan-2013) 8 44 1 0 LNP, central (Dec-2013) 20 29 2 1 LANP (Oct-2014) 0 25 0 1 LANP (Feb-2013) 0 0 0 0 Sarcophagidae  Oxysarcodexia varia LPNP (Jan-2011) 342 88 72 21 LPNP (Jan-2012) 13 31 4 4 LNP, southern (Feb-2011) 15 40 7 6 LNP, northern (Jan-2013) 55 34 20 4 LNP, central (Dec-2013) 38 17 2 4 LANP (Oct-2014) 11 44 6 5 LANP (Feb-2013) 0 0 1 0  Microcerella spinigena LPNP (Jan-2011) 1 7 14 13 LPNP (Jan-2012) 28 23 12 9 LNP, southern (Feb-2011) 1 13 18 14 LNP, northern (Jan-2013) 9 17 20 17 LNP, central (Dec-2013) 8 20 2 2 LANP (Oct-2014) 34 88 36 22 LANP (Feb-2013) 0 1 20 4 Muscidae  Hydrotaea acuta LPNP (Jan-2011) 13 68 1 0 LPNP (Jan-2012) 0 3 0 0 LNP, southern (Feb-2011) 14 80 2 0 LNP, northern (Jan-2013) 6 19 0 0 LNP, central (Dec-2013) 0 4 0 0 LANP (Oct-2014) 1 8 0 0 LANP (Feb-2013) 0 0 0 0 Species Site (date) Baited trap Active capture ♂ ♀ ♂ ♀ Calliphoridae  Sarconesia magellanica LPNP (Jan-2011) 21 32 7 4 LPNP (Jan-2012) 100 92 9 5 LNP, southern (Feb-2011) 85 59 14 4 LNP, northern (Jan-2013) 9 13 0 0 LNP, central (Dec-2013) 2 1 0 0 LANP (Oct-2014) 49 56 0 3 LANP (Feb-2013) 0 0 0 0  Calliphora vicina LPNP (Jan-2011) 26 37 12 8 LPNP (Jan-2012) 14 26 5 6 LNP, southern (Feb-2011) 14 14 1 1 LNP, northern (Jan-2013) 0 0 0 0 LNP, central (Dec-2013) 1 2 0 1 LANP (Oct-2014) 0 12 0 1 LANP (Feb-2013) 56 72 27 29  Compsomyiops fulvicrura LPNP (Jan-2011) 2 14 3 1 LPNP (Jan-2012) 16 24 1 0 LNP, southern (Feb-2011) 2 4 1 0 LNP, northern (Jan-2013) 8 44 1 0 LNP, central (Dec-2013) 20 29 2 1 LANP (Oct-2014) 0 25 0 1 LANP (Feb-2013) 0 0 0 0 Sarcophagidae  Oxysarcodexia varia LPNP (Jan-2011) 342 88 72 21 LPNP (Jan-2012) 13 31 4 4 LNP, southern (Feb-2011) 15 40 7 6 LNP, northern (Jan-2013) 55 34 20 4 LNP, central (Dec-2013) 38 17 2 4 LANP (Oct-2014) 11 44 6 5 LANP (Feb-2013) 0 0 1 0  Microcerella spinigena LPNP (Jan-2011) 1 7 14 13 LPNP (Jan-2012) 28 23 12 9 LNP, southern (Feb-2011) 1 13 18 14 LNP, northern (Jan-2013) 9 17 20 17 LNP, central (Dec-2013) 8 20 2 2 LANP (Oct-2014) 34 88 36 22 LANP (Feb-2013) 0 1 20 4 Muscidae  Hydrotaea acuta LPNP (Jan-2011) 13 68 1 0 LPNP (Jan-2012) 0 3 0 0 LNP, southern (Feb-2011) 14 80 2 0 LNP, northern (Jan-2013) 6 19 0 0 LNP, central (Dec-2013) 0 4 0 0 LANP (Oct-2014) 1 8 0 0 LANP (Feb-2013) 0 0 0 0 View Large Capture Rate The effects of the trapping method on the capture rate showed no significant differences for O. varia (CR baited trap: 0.036 ± 0.051; CR active capture: 0.022 ± 0.026; T paired test =1.53, P = 0.175); S. magellanica (CR baited trap: 0.036 ± 0.053; CR active capture: 0.008 ± 0.010; T paired test =1.71, P = 0.138); and C. vicina (CR baited trap: 0.015 ± 0.015; CR active capture: 0.019 ± 0.031; T paired test = −0.489, P = 0.635). The effect of trapping method was significant on the capture rate for M. spinigena, with higher capture rates observed for the active capture (CR baited trap: 0.014 ± 0.015; CR active capture: 0.037 ± 0.025; T paired test = −3.06, P = 0.022). Regression analysis indicated positive relationship between both methods in all cases. These results were significant for O. varia (r2 = 0.976, F(1,5) = 209.04, P < 0.001), S. magellanica (r2 = 0.897, F(1,5) = 43.63, P = 0.001), and C. vicina (r2 = 0.644, F(1,5) = 9.04, P = 0.030), while M. spinigena showed no significant linear regression (r2 = 0.411, F(1,5) = 3.49, P = 0.121; Fig. 2). Fig. 2. View largeDownload slide Relationship between capture rates of baited traps and active captures for sarcosaprophagous species of Valdivian temperate forests of South America. Dashed lines indicate slope equal to 1. Fig. 2. View largeDownload slide Relationship between capture rates of baited traps and active captures for sarcosaprophagous species of Valdivian temperate forests of South America. Dashed lines indicate slope equal to 1. Sex Ratio To compare the sex ratio patterns between the two sampling methods, four species were captured in acceptable numbers in both (Fig. 3). A general trend of strong female-biased sex ratio was obtained for baited traps, whereas higher proportions of males were detected for active capture. However, significant differences were detected only for M. spinigena (T paired test = −3.30, P = 0.029) and S. magellanica (T paired test = −5.44, P = 0.032). In the case of C. fulvicrura and H. acuta, no comparisons were performed in order of the low frequency obtained in samples based on active capture. However, the sex ratio obtained with baited traps for C. fulvicrura (Pf = 0.78 ± 0.17, n = 5) and H. acuta (Pf = 0.82 ± 0.05, n = 3) was also female biased. Fig. 3. View largeDownload slide Sex ratio comparison between baited traps (orange) and active captures (blue) for sarcosaprophagous species of Valdivian temperate forests of South America. Fig. 3. View largeDownload slide Sex ratio comparison between baited traps (orange) and active captures (blue) for sarcosaprophagous species of Valdivian temperate forests of South America. The linear models indicate that capture rate of males increased with that of females irrespectively of the trapping method employed (Table 3). The only exception to this pattern was no significant result obtained for captures of O. varia with baited traps. A lower coefficient value was observed for the models based on the baited trap than models based on active capture, indicating a stronger female bias for the former collecting method. Models based on active capture for C. fulvicrura and H. acuta were not calculated due to the extremely low captures associated with such method. Table 3. Linear regression coefficients of female capture rate in relation to male capture rate obtained with baited traps and active captures for sarcosaprophagous Calyptratae of Valdivian temperate forest of South America Species Baited trap Active capture r2 Coefficient P r2 Coefficient P Calliphoridae  Sarconesia magellanica 0.98 1.10 (±0.06) <0.001 0.67 1.66 (±0.52) 0.024  Calliphora vicina 0.91 0.67 (±0.09) <0.001 0.98 0.94 (±0.05) <0.001  Compsomyiops fulvicrura 0.71 0.60 (±0.17) 0.017 — — — Sarcophagidae  Oxysarcodexia varia 0.52 2.86 (±1.22) 0.065 0.76 3.30 (±0.52) 0.010  Microcerella spinigena 0.60 0.70 (±0.25) 0.040 0.69 1.40 (±0.42) 0.020 Muscidae  Hydrotaea acuta 0.97 0.18 (±0.01) <0.001 — — — Species Baited trap Active capture r2 Coefficient P r2 Coefficient P Calliphoridae  Sarconesia magellanica 0.98 1.10 (±0.06) <0.001 0.67 1.66 (±0.52) 0.024  Calliphora vicina 0.91 0.67 (±0.09) <0.001 0.98 0.94 (±0.05) <0.001  Compsomyiops fulvicrura 0.71 0.60 (±0.17) 0.017 — — — Sarcophagidae  Oxysarcodexia varia 0.52 2.86 (±1.22) 0.065 0.76 3.30 (±0.52) 0.010  Microcerella spinigena 0.60 0.70 (±0.25) 0.040 0.69 1.40 (±0.42) 0.020 Muscidae  Hydrotaea acuta 0.97 0.18 (±0.01) <0.001 — — — Significant values (P < 0.05) are shown in bold. View Large Table 3. Linear regression coefficients of female capture rate in relation to male capture rate obtained with baited traps and active captures for sarcosaprophagous Calyptratae of Valdivian temperate forest of South America Species Baited trap Active capture r2 Coefficient P r2 Coefficient P Calliphoridae  Sarconesia magellanica 0.98 1.10 (±0.06) <0.001 0.67 1.66 (±0.52) 0.024  Calliphora vicina 0.91 0.67 (±0.09) <0.001 0.98 0.94 (±0.05) <0.001  Compsomyiops fulvicrura 0.71 0.60 (±0.17) 0.017 — — — Sarcophagidae  Oxysarcodexia varia 0.52 2.86 (±1.22) 0.065 0.76 3.30 (±0.52) 0.010  Microcerella spinigena 0.60 0.70 (±0.25) 0.040 0.69 1.40 (±0.42) 0.020 Muscidae  Hydrotaea acuta 0.97 0.18 (±0.01) <0.001 — — — Species Baited trap Active capture r2 Coefficient P r2 Coefficient P Calliphoridae  Sarconesia magellanica 0.98 1.10 (±0.06) <0.001 0.67 1.66 (±0.52) 0.024  Calliphora vicina 0.91 0.67 (±0.09) <0.001 0.98 0.94 (±0.05) <0.001  Compsomyiops fulvicrura 0.71 0.60 (±0.17) 0.017 — — — Sarcophagidae  Oxysarcodexia varia 0.52 2.86 (±1.22) 0.065 0.76 3.30 (±0.52) 0.010  Microcerella spinigena 0.60 0.70 (±0.25) 0.040 0.69 1.40 (±0.42) 0.020 Muscidae  Hydrotaea acuta 0.97 0.18 (±0.01) <0.001 — — — Significant values (P < 0.05) are shown in bold. View Large Discussion Insect sampling requires knowledge of their biology, preferred habitats, and activity patterns. As a rule, a good sampling technique that is replicable, accurate, and less operator-dependent is useful for monitoring programs or general research on ecological populations of sarcosaprophagous Calyptratae (Lysyk and Axtell 1986, Gerry et al. 2011). In contrast, field recording techniques and protocols for taxonomic inventories are often associated to direct catches made by taxonomist. In fact, direct capture of fly specimens for taxonomic purposes is a common practice applied by entomologists to preserve high-quality samples of specimens for taxonomy. Both ecological and taxonomic research on sarcosaprophagous Calyptratae are highly required given their sanitary and forensic implications of the species, and both types of sampling techniques are widely used to study sarcosaprophagous fly populations. This study showed that besides the expected interspecific differences in trapping efficiency and biases, there are acute intraspecific differences between sampling methods. Some studies indicate that fly monitoring methods accumulating individuals over time, such as traps, provide more reliable estimates of fly abundance and activity relative to instantaneous visual counts (or catches), which are subject to diel or changing environmental conditions (Lysyk and Moon 1994). Taking into account the applied methodology, the results obtained with active captures could be partly modified as a consequence of simultaneous use of baited traps in the field. In fact, our study cannot discriminate whether the presence of bait would affect the associated active captures in the same areas. However, the application of both methods at the same time ensures the avoidance of daily-changing environmental conditions, which strongly affect flying insects. For this study, we avoid long-term exposures of baits (e.g., 24–48 h) to prevent the attractant effect on flies from far areas, promoting only the concentration of specimens from the closer surrounding areas into the traps. Such short-time collecting may be a good indicator of local abundance of species and probably less affecting active captures. Although our data have been obtained during the warm season of the year, which is equivalent to the period of peaks and outbreaks of dipteran abundance, a certain degree of seasonal bias may be affecting the sex ratio. Thus, samples of October seem to be comparatively more strongly female-biased and hence may reflect other differences of behavior of sexes (e.g., by differential emergence of adults). These observations must be taken into account and put into a context in future studies on the sex ratio along different seasons of the year. Our results show that the estimation of sex ratio for sarcosaprophagous flies is determined by the interactions between biological characteristic of each species and sampling methodology. The sex ratios of every species depend on several factors such as reproductive characteristics, resources availability and use, level of competition between species, among others. Therefore, it is difficult to find patterns in the sex ratio of the species, so the sex ratio can be analyzed for each species and environmental context. Two species resulted noticeably reluctant to active captures, C. fulvicrura and H. acuta. In the case of C. fulvicrura, males are frequently seen sun-basking on stones or directly on soil, but they are difficult to catch with entomological net. In the case of H. acuta, individuals of this species are small species and probably display inconspicuous behaviors, hence may be overlooked during the active capture by collectors. In addition, the discrepancy between the abundance patterns established by different capture methods is particularly important, as it may reflect the conflict of interest of the sexes and their differences in behavior. The mating system of the species, asymmetry in parental investment, and the differences in the protein requirements of the sexes to reach sexual maturity may play an important role in the observed sex ratios. Unlike male, females seek for decaying organic matter as breeding substrate and as nutritional resource. Physiological reproductive state influences female behavior, which depend on protein intakes to reach their ovarian development (Stoffolano et al. 1990, 1995). These factors may explain the higher prevalence of females in baited traps, which are skewed by the presence of immature females searching for protein sources and gravid females searching for oviposition or larviposition sites. Previous studies indicate that the general pattern observed in Sarcophagidae, and specifically in O. varia, has provided male-biased samples when animal-origin baits are used to capture them (Mariluis et al. 2007, Mulieri et al 2011, Mulieri et al. 2015a). In our study, this trend was not clearly observed although both sarcophagid species analyzed here, O. varia and M. spinigena, showed a comparatively higher proportion of males than calliphorid species. Also, both sarcophagids showed significantly higher deviations in their sex ratios. O. varia is a species that usually exhibits outbreaks in late spring and summer, and whose peaks of abundance may reflect the emergence of successive fly generations (Henning et al. 2005). Differences on emergence of sexes, influenced by environmental and weather condition, may explain its highly fluctuating sex-bias phenotypes. Male blowflies, house flies, and flesh flies establish perch sites in vegetation, stones, or other similar landmarks and wait for females to potential mating (Thomas 1950, Land and Collett 1974, Downes 1994, Paquette et al. 2008). Such hilltopping behavior in which the males perch on these landmarks devoid of resources for females provide a strategy for mating encounters and may have strong influence on male-biased samples made with entomological net under the active capture method. Baited traps with putrescine are more efficient method to sample sarcosaprophagous Calyptratae, due to its high specificity, diversity, and capture rate obtained in comparison to active captures (Olea et al. 2017). However, despite these differences in efficacy and their associated potential biases, fluctuations in fly abundance show an existing relationship between both sampling methods and, therefore, can be inferred to reflect the local abundance of the species analyzed. Indeed, coincidence of results obtained by both methods on the abundance fluctuations of analyzed species has indicated that the use of baited traps with putrescine is suitable for ecological researches and monitoring programs of Calyptratae of medical and veterinary impact. Our study also raises some general patterns of behavior in sarcosaprophagous Calyptratae. We show that the common behavior of female-biased captures with bait is likely to correspond to species whose male display a perch behavior, being the latter well reflected by active captures. Further work is needed to establish the behavioral basis of territoriality and perching behavior of males and its relation to the sites of harassment to female (e.g., occurring on food resources or nonresource territories). Such studies in association with the physiological requirements to reach reproductive maturity of females would provide valuable observations on factors underlying our patterning observations. Acknowledgments We gratefully acknowledge the financial support from CONICET and ANPCyT (PIP 11220090100548, PICT-2008-0094, PICT-2011-0490). We are grateful to the personnel of ‘Administración de Parques Nacionales’ for their valuable logistical support during the field work. References Cited Baz , A. , B. Cifrián , L. M. Díaz-Aranda , and D. Martín-Vega . 2007 . The distribution of adult blow-flies (Diptera: Calliphoridae) along an altitudinal gradient in central Spain . Ann. Soc. Entomol. Fr. (n.s.) . 43 : 289 – 296 . Google Scholar CrossRef Search ADS Brown , B. V. , A. Borkent , J. M. Cumming , D. M. Wood , N. E. Woodley , and M. A. Zumbado . 2009 . Manual of central American dıptera , v ol. 1 . NRC Research Press , Ottawa, Ontario, Canada . Centeno , N. , D. Almorza , and C. Arnillas . 2004 . Diversity of Calliphoridae (Insecta: Diptera) in Hudson, Argentina . Neotrop. Entomol . 33 : 387 – 390 . Google Scholar CrossRef Search ADS Downes , Jr, W. L . 1994 . 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TI - Sex Ratio and Abundance Fluctuations of Sarcosaprophagous Calyptratae (Diptera): Field Evaluation of Two Sampling Techniques
JF - Journal of Medical Entomology
DO - 10.1093/jme/tjy093
DA - 2018-09-01
UR - https://www.deepdyve.com/lp/oxford-university-press/sex-ratio-and-abundance-fluctuations-of-sarcosaprophagous-calyptratae-y1M3VrK6eP
SP - 1210
EP - 1216
VL - 55
IS - 5
DP - DeepDyve
ER -