Is a starving host tastier? Reprodu

Is a starving host tastier? Reproduction in fleas
parasitizing food-limited rodents

We hypothesized that food availability, and therefore body condition, of a rodent host, Meriones crassus, affects egg production and survival, and development time of preimago and adults of the first generation of the flea Xenopsylla ramesis
2.Egg production was significantly higher in fleas parasitizing underfed than control
animals.
3.Food availability for hosts affected survival of eggs and larvae produced by fleas on
these rodents, but did not affect survival of pupae. More than twice the number of eggs
from fleas on food-limited hosts survived than those from fleas on control rodents.
Highest larval survival was recorded in fleas on rodents with 30% of maintenance
energy intake.
4.Survival of new generation imagos was lowest in fleas from parents on hosts with
the highest food limitation. By contrast, survival of parent fleas was highest on hosts
offered 30% of maintenance energy intake.
5.Time of egg and larval development was longest on hosts consuming 30% of energy
requirements for maintenance. By contrast, there was no difference in time to emergence
in pupae from flea females on rodents from different treatments. Survival time
under starvation of imago of the first generation was shortest in offspring of fleas that parasitized M. crassus offered the minimal amount of food. The opposite was true for parent fleas.
6.The results suggest nutritional and/or energetic cost of host resistance, measured
as host-mediated parasite fitness loss, as well as possible adaptive stress-induced
immunosuppression.
Key-words
: Egg production, flea, food limitation, rodent host, survival
Functional Ecology
(2005)
Introduction
Distribution of parasite individuals across a host population is characterized by their aggregation. Most individuals of the parasite occur on a few host individuals, while most host individuals have only a few, if any, parasites (Anderson & May 1978). The general cause of the heterogeneous distribution of parasites is due to host heterogeneity of the rate of gain or loss of parasitesPoulin 1998). In other words, if some hosts have more parasites than would be predicted by chance, it suggests that they offer the parasites a better quality habitat. In particular, intraspecific host variation in suitability for a parasite can be caused by the variation in the pattern
of resource acquisition by a parasite such as intrahost variation in defences.
Hosts defend themselves against parasites using specific behavioural, physiological and/or immunological mechanisms that can result in loss of fitness in the parasites. This host-mediated loss of fitness in a parasite is considered to be host resistance (Poulin 1998). The defence against parasites can be costly for a host. For example, activation of an immune response and even maintenance of a competent immune system is an energetically demanding process that requires trade-off decisions
among competing energy demands for growth, reproduction, thermoregulation, work and immunity(Sheldon & Verhulst 1996). Empirical evidence suggests that such costs can be high (e.g. Moret & Schmid- Hempel 2000). The trade-off between the advantage of resistance and its cost should be most critical for hosts that face energy limitations. Therefore, energy-deprived hosts might be less resistant and, thus, represent better patches for parasites. Intraspecific host variation in energy reserves can arise due to a variety of reasons (Kam & Degen 1993; Cumming & Bernard 1997). As a result, in many nontropical vertebrate animals, disease prevalence is increased during periods of food shortage compared with periods when food is readily available (Lochmiller, Vestey &
McMurray 1994). However, resources that parasites extract from their hosts (e.g. blood) can be of a lower quality in energy-deprived hosts (De Pedro et al. 2003).
Thus, hosts in good condition can be a better food source than hosts in poor condition (Dawson & Bortolotti 1997).
Consequently, parasites face a trade-off between the choice to attack less defended but lower-quality,vs more defended but higher-quality, hosts. From the evolutionary
perspective, the strategy of parasitizing either energy deprived or energy-rich hosts would depend on relative fitness rewards from exploiting these hosts. This reasoning leads to two alternative predictions regarding the effect of host energy deprivation on
reproductive patterns of a parasite. Reproductive output of a parasite will be higher when exploiting energy deprived hosts if the fitness increment due to reduced host defences is higher than the fitness decline due to lower quality of resources extracted from a host. Alternatively, this reproductive output will be lower when exploiting energy deprived hosts if the fitness increment due to reduced host defences is lower than the fitness decline due to lower quality of extracted resources.
The effect of body condition of hosts on their resistance to parasites has been studied in a variety of animals by manipulating the body condition of hosts (Oppliger, Christe & Richner 1996; Brown, Loosli & Schmid-Hempel 2000; Jokela et al . 2005). However, all
of these studies have investigated this phenomenon from the host perspective, whereas the effect of host condition on parasite parameters (apart for abundance) has largely
been neglected. Here, we studied the effect of host energy intake on parasite fitness. We hypothesized that food limitation of a rodent host, Meriones crassus, affects reproductive potential (in terms of egg production) and quality of offspring (in terms of survival and development time of preimaginal stages and adults of the first generation) of its characteristic flea parasiteXenopsylla ramesis. Fleas (Siphonaptera) are parasites of higher vertebrates, being most abundant and diverse on small mammals.
In most cases, preimaginal development is entirely off-host. Larvae of almost all flea species are not parasitic and feed on organic debris in the burrow and/ or nest of the host.

Materials and methods
Fleas and rodents (27 adult males) were obtained from our laboratory colonies started from field-collected individuals. Details on the flea and rodent-rearing procedures can be found elsewhere (Krasnov et al. 2001a,b, 2004). In this study we used only newly emerged fleas, 2 days of age, which did not feed from emergence until experimental treatments. The study was conducted under permits from the Israel Nature and National
Parks Protection Authority and Ben-Gurion University Committee for the Ethical Care and Use of Animals in Experiments.

food limitation treatments
Prior to experimental trials with fleas, the rodents were placed in individual plastic cages (20×40×15 cm3 with 3 mm clean sand as a substrate) and divided randomly into three groups (nine individuals per group). One group (control group, C) was offered millet seeds equivalent to approximately 100% of maintenance energy requirements,
whereas the two other groups were offered 60% (group T1) and 30% (group T2), respectively, of maintenance requirements. In addition, rodents were offered 3 g fresh alfalfa leaves, which provided their water needs but with minimal additional energy (I. Khokhlova, unpublished data). Energy requirements for maintenance of
M. crassus were taken as 8·3 kJ day−1(Khokhlova, Degen & Kam 1995) and calculated for
each animal based on its body mass (mb). Animals were weighed daily at 09.00 h to 0·01g(Ohaus CT200-Selectronic balance, Ohaus Corporation, Pine Brook, NJ,USA). Food offered was weighed to 0·0001 g (Mettler-Toledo AB, Dietikon, Switzerland). Animals from thecontrol group and animals from the T1 treatment maintained their body mass throughout the experimental period; their body mass after the first week was 98·9±2·1% and 97·3±1·7%, respectively, of initial body mass. However, body mass of rodents from the T2 group decreased after the first week to 81·1 ± 1·8% of initial body mass.

manipulation with fleas

We selected 945 newly emerged female and 270 newly emerged male X. ramesis and assigned them randomly to the three experimental treatments that differed in food availability to a rodent host. We placed 35 female and 10 male fleas on each rodent a week after the beginning of experiments. Four days after the fleas were in the rodent cage, we collected the fleas by brushing the hairof the rodent with a toothbrush and sieving the cage substrate until no fleas could be recovered during 10 min of either brushing or sieving. No behavioural difference during manipulations was recorded among rodents of the three experimental groups. In total, we recovered 804 female and 156 male fleas. Each female flea was examined under a light microscope, and the degree of egg development (early, middle or late stage) was determined visually (see Krasnov et al. 2002 for details). Fleas with egg

Results (Indonesian) 1:

Apakah sebuah host yang kelaparan lebih lezat? Reproduksi di kutuparasitizing makanan terbatas tikusKami hipotesis bahwa ketersediaan pangan, dan karenanya mempengaruhi kondisi tubuh, sejumlah hewan pengerat, Meriones crassus, produksi telur dan kelangsungan hidup, dan waktu pengembangan dari preimago dan orang dewasa dari generasi pertama flea Xenopsylla ramesis2. telur produksi adalah signifikan lebih tinggi di kutu parasitizing kurang makan dari kontrolhewan.3. ketersediaan pangan host mempengaruhi kelangsungan hidup telur dan larva diproduksi oleh kutu padatikus ini, tetapi tidak mempengaruhi kelangsungan hidup kepompong. Lebih dari dua kali jumlah telurdari kutu pada makanan-terbatas host selamat daripada dari kutu pada pengendalian tikus.Kelangsungan hidup larva tertinggi tercatat di kutu pada tikus dengan 30% dari pemeliharaanasupan energi.4. kelangsungan hidup generasi baru imagos yang terendah di kutu dari orangtua pada host denganbatasan makanan yang tertinggi. Sebaliknya, kelangsungan hidup kutu orangtua adalah tertinggi pada hostditawarkan 30% dari asupan energi pemeliharaan.5. kali telur dan perkembangan larva adalah terpanjang di host mengkonsumsi 30% dari energipersyaratan untuk pemeliharaan. Sebaliknya, ada tidak ada perbedaan dalam waktu untuk timbulnyadalam kepompong dari loak betina pada tikus dari perawatan yang berbeda. Waktu kelangsungan hidupdi bawah kelaparan imago generasi pertama adalah terpendek dalam keturunan kutu yang parasitized M. crassus ditawarkan minimal jumlah makanan. Sebaliknya adalah benar untuk orangtua kutu.6. hasil menunjukkan biaya gizi dan/atau energik resistensi host, diukursebagai tuan rumah-dimediasi parasit kebugaran kerugian, serta mungkin adaptif diinduksi stresimunosupresi.Kata kunci: Telur produksi, kutu, batasan makanan, hewan pengerat host, kelangsungan hidupEkologi fungsional(2005)PendahuluanDistribusi parasit individu di seluruh populasi inang dicirikan oleh agregasi mereka. Kebanyakan individu parasit terjadi pada beberapa host individu, sementara kebanyakan host individu memiliki hanya sedikit, jika ada, parasit (Anderson & Mei 1978). Penyebab umum distribusi heterogen parasit adalah karena heterogenitas host tingkat keuntungan atau kerugian dari parasitesPoulin 1998). Dengan kata lain, jika beberapa host memiliki parasit lain daripada akan dapat diprediksi secara kebetulan, itu menunjukkan bahwa mereka menawarkan parasit habitat kualitas lebih baik. Secara khusus, intraspecific host variasi dalam kesesuaian untuk parasit dapat disebabkan oleh variasi dalam polasumber daya akuisisi oleh parasit seperti intrahost variasi dalam pertahanan.Host membela diri melawan menggunakan mekanisme perilaku, fisiologis dan/atau imunologi tertentu yang dapat mengakibatkan hilangnya kebugaran di parasit parasit. Kerugian ini host-dimediasi kebugaran di parasit dianggap resistensi host (Poulin 1998). Pertahanan terhadap parasit dapat menjadi mahal bagi tuan rumah. Sebagai contoh, aktivasi respon imun dan bahkan pemeliharaan sistem kekebalan tubuh yang kompeten adalah suatu proses yang menuntut penuh semangat yang membutuhkan trade-off keputusanamong competing energy demands for growth, reproduction, thermoregulation, work and immunity(Sheldon & Verhulst 1996). Empirical evidence suggests that such costs can be high (e.g. Moret & Schmid- Hempel 2000). The trade-off between the advantage of resistance and its cost should be most critical for hosts that face energy limitations. Therefore, energy-deprived hosts might be less resistant and, thus, represent better patches for parasites. Intraspecific host variation in energy reserves can arise due to a variety of reasons (Kam & Degen 1993; Cumming & Bernard 1997). As a result, in many nontropical vertebrate animals, disease prevalence is increased during periods of food shortage compared with periods when food is readily available (Lochmiller, Vestey &McMurray 1994). However, resources that parasites extract from their hosts (e.g. blood) can be of a lower quality in energy-deprived hosts (De Pedro et al. 2003).Thus, hosts in good condition can be a better food source than hosts in poor condition (Dawson & Bortolotti 1997).Consequently, parasites face a trade-off between the choice to attack less defended but lower-quality,vs more defended but higher-quality, hosts. From the evolutionaryperspective, the strategy of parasitizing either energy deprived or energy-rich hosts would depend on relative fitness rewards from exploiting these hosts. This reasoning leads to two alternative predictions regarding the effect of host energy deprivation onreproduksi pola parasit. Reproduksi output dari parasit akan lebih tinggi ketika pemanfaatan energi dirampas host jika kenaikan kebugaran karena pertahanan tuan rumah dikurangi lebih tinggi dari penurunan kebugaran karena kualitas lebih rendah sumber daya yang diekstrak dari sebuah host. Selain itu, output reproduksi ini akan lebih rendah ketika pemanfaatan energi dirampas host jika kenaikan kebugaran karena pertahanan tuan rumah dikurangi lebih rendah dari penurunan kebugaran karena kualitas lebih rendah daya diekstrak.Efek kondisi tubuh host pada perlawanan mereka untuk parasit telah dipelajari di berbagai hewan dengan memanipulasi kondisi tubuh host (Oppliger, Christe & Richner tahun 1996; Brown, Loosli & Schmid-Hempel 2000; Jokela et al. 2005). Namun, Semuastudi ini telah menyelidiki fenomena ini dari perspektif tuan rumah, sedangkan efek host kondisi pada parameter parasit (terpisah untuk kelimpahan) memiliki sebagian besartelah diabaikan. Di sini, kita mempelajari efek dari asupan energi host di parasit kebugaran. Kami hipotesis bahwa pembatasan makanan sejumlah hewan pengerat, Meriones crassus, mempengaruhi potensi reproduksi (dalam hal produksi telur) dan kualitas keturunan (kelangsungan hidup dan pengembangan waktu dari tahapan preimaginal) dan orang dewasa dari generasi pertama yang khas loak parasiteXenopsylla ramesis. Kutu (Siphonaptera) adalah parasit vertebrata yang lebih tinggi, yang paling berlimpah dan beragam pada mamalia kecil.In most cases, preimaginal development is entirely off-host. Larvae of almost all flea species are not parasitic and feed on organic debris in the burrow and/ or nest of the host.Materials and methodsFleas and rodents (27 adult males) were obtained from our laboratory colonies started from field-collected individuals. Details on the flea and rodent-rearing procedures can be found elsewhere (Krasnov et al. 2001a,b, 2004). In this study we used only newly emerged fleas, 2 days of age, which did not feed from emergence until experimental treatments. The study was conducted under permits from the Israel Nature and NationalParks Protection Authority and Ben-Gurion University Committee for the Ethical Care and Use of Animals in Experiments.food limitation treatmentsPrior to experimental trials with fleas, the rodents were placed in individual plastic cages (20×40×15 cm3 with 3 mm clean sand as a substrate) and divided randomly into three groups (nine individuals per group). One group (control group, C) was offered millet seeds equivalent to approximately 100% of maintenance energy requirements,whereas the two other groups were offered 60% (group T1) and 30% (group T2), respectively, of maintenance requirements. In addition, rodents were offered 3 g fresh alfalfa leaves, which provided their water needs but with minimal additional energy (I. Khokhlova, unpublished data). Energy requirements for maintenance ofM. crassus diambil sebagai 8·3 kJ day−1 (Khokhlova, Degen & Kam 1995) dan dihitung untukmasing-masing hewan berdasarkan massa tubuh (mb). Hewan ditimbang setiap hari jam 09.00 h untuk 0·01g (Ohaus CT200-Selectronic keseimbangan, Ohaus Corporation, Pine Brook, NJ, USA). Makanan yang ditawarkan ditimbang untuk 0·0001 g (AB Mettler Toledo, Dietikon, Swiss). Hewan dari thecontrol group dan binatang dari pengobatan T1 mempertahankan massa tubuh mereka selama percobaan; tubuh mereka massa setelah minggu pertama adalah 98·9±2·1% dan 97·3±1·7%, masing-masing, dari awal massa tubuh. Namun, massa tubuh tikus dari kelompok T2 menurun setelah minggu pertama 81·1 ± 1·8% dari awal massa tubuh.manipulasi dengan kutuWe selected 945 newly emerged female and 270 newly emerged male X. ramesis and assigned them randomly to the three experimental treatments that differed in food availability to a rodent host. We placed 35 female and 10 male fleas on each rodent a week after the beginning of experiments. Four days after the fleas were in the rodent cage, we collected the fleas by brushing the hairof the rodent with a toothbrush and sieving the cage substrate until no fleas could be recovered during 10 min of either brushing or sieving. No behavioural difference during manipulations was recorded among rodents of the three experimental groups. In total, we recovered 804 female and 156 male fleas. Each female flea was examined under a light microscope, and the degree of egg development (early, middle or late stage) was determined visually (see Krasnov et al. 2002 for details). Fleas with egg